Hold the Phone It's like a classic horror movie scene: a scientist using amazing technology in an attempt to reanimate parts of dead bodies, seeking out nature's secrets. But when the young Hungarian engineer Georg von Békésy started experimenting with cadavers in the 1920s, he was not trying to create life. He was seeking to answer a practical question: Why are human ears so much more sensitive than most microphones? Békésy thought that learning how the human ear works might allow him to make a better microphone for his employer, the Hungarian phone company. He gathered cadavers from local hospitals and came up with a clever dissection that would reveal the inner ear without destroying it. (His work was not always appreciated by his fellow engineers; they didn't
like finding their drill press full of human bone dust in the morning.) Bringing his background in physics to bear, Békésy devised exquisitely precise physical models and biophysical experiments that let him measure extremely brief, minuscule movements in the inner ear. His subsequent discoveries provided us with the key to understanding how we translate a stream of auditory data--sounds--into neural activity that the brain can understand. In the end, Békésy did not come up with a better microphone, but his discoveries have helped restore hearing to thousands of people who once were deaf, as we'll see in this chapter.
Your existence is directly attributable to the keen senses possessed by your distant ancestors--senses that enabled them to find food and mates and to avoid predators and other dangers. In this chapter we consider some of the incredible sensors that let us monitor important signals from distant sources, especially sounds (by audition) and smells (by olfaction). We also discuss related systems for detecting position and movement of the body (the vestibular system, related to the auditory system) and tastes of foods (the gustatory or taste sense, which like olfaction is a chemical sense). We begin with hearing, because audition evolved from special mechanical receptors related to the touch system that we discussed in Chapter 5.
178CHAPTER6 View Animation 6.2: Brain Explorer The Ears Have It The external ears, or pinnae, of mammals come in a variety of shapes, each adapted to a particular ecological niche. Many mammals can move their ears to direct them toward a particular sound. In such cases, the brain must account for the position of the ear to judge where a particular sound came from. (Fennec fox [top left]; whispering bat [top right]; sea otter [bottom left]; chimpanzee [bottom right].)
6.1Hearing: Pressure Waves in the Air Are Perceived as Sound The first part of the chapter is concerned with the structure and function of the ear, especially the inner ear, which gives us our sense of hearing. After reading this section, you should be able to: 6.1.1 Explain how the external ear and middle ear capture and concentrate sound energy and convey it to the inner ear. 6.1.2 Sketch the anatomy of the middle and inner ears, highlighting the location of sensorineural components. 6.1.3 Explain how vibrations travel through the cochlea and how they are converted into neural activity. 6.1.4 Describe the process by which the organ of Corti encodes the frequencies of sounds. 6.1.5 Summarize the neural projections between the cochlea and brain. 6.1.6 Identify the principal auditory pathways and structures of the brain, and describe the integration of signals from the left and right ears. 6.1.7 Describe the orderly map of frequencies found at each level of the auditory system.
decibel (dB) A measure of sound intensity, perceived as loudness. hertz (Hz) Cycles per second, as of an auditory stimulus. Hertz is a measure of frequency. transduction The conversion of one form of energy to another.
Hearing is vital for the survival of most animals. Humans can produce an impressive variety of vocalizations--from barely audible murmurs to soaring flights of song--but we especially rely on speech sounds for our social relations and for the transmission of knowledge between individuals. Across the animal kingdom, species produce and perceive sounds in wildly different ways, shaped by their unique evolutionary history. Birds sing and crickets chirp in order to attract mates, while monkeys grunt and screech and burble to signal comfort, danger, and pleasure. Owls and bats exploit the directional property of sound to locate prey and avoid obstacles in the dark, because unlike light, sound can be detected in the darkest night, or even around a corner. How does energy transmitted through air become the speech, music, and other sounds we hear? Your auditory system detects changes in the vibration of air molecules that are caused by sound sources: it senses both the intensity of sounds, measured in decibels (dB) and perceived as loudness, and their frequency, measured in cycles per second, or hertz (Hz), and perceived as pitch. BOX 6.1 describes some of the basic properties of sound that are relevant to our discussion of hearing. The outer ear directs sound into the inner parts of the ear, where the mechanical force of sound is transduced into neural activity: the action potentials that inform the brain. Your ears are incredibly sensitive
pure tone A tone with a single frequency of vibration. amplitude Also called intensity. The force that sound exerts per unit area, which we experience as loudness. frequency The number of cycles per second in a sound wave, measured in hertz. fundamental The predominant frequency of an auditory tone. harmonic A multiple of a particular frequency called the fundamental. timbre The characteristic sound quality of a musical instrument, as determined by the relative intensities of its various harmonics.
BOX 6.1 The Basics of Sound
We perceive a repetitive pattern of local increases and decreases in air pressure as sound. Usually this oscillation is caused by a vibrating object, such as a loudspeaker or a person's larynx during speaking. A single alternation of compression and expansion of air is called one cycle.
The figure illustrates the oscillations in pressure produced by a vibrating loudspeaker. Because the sound produced by the loudspeaker here has only one frequency of vibration, it is called a pure tone and can be represented by a sine wave. A pure tone is described physically in terms of two measures:
Amplitude and frequency of sound waves Vibrating body (loudspeaker) Vibration Wavelength, one cycle
Compression and expansion of air molecules produced by the loudspeaker's vibration Amplitude: representation of the pressure waves above
Greater amplitude of vibration Greater frequency of vibration
Stronger vibration produces larger changes in pressure; no change in frequency Amplitude same as original; frequency doubled
Amplitude Also called intensity, this is usually measured as sound pressure in dynes per square centimeter (dyn/cm2). Our perception of amplitude is termed loudness, expressed as decibels (dB). The decibel scale is logarithmic: one decibel is the threshold for human hearing, a whisper is about 20 dB, and a departing jetliner a couple of hundred feet overhead--a sound a million times as intense--is about 120 dB. Frequency This is the number of cycles per second, measured in hertz (Hz). So, middle A on a piano has a frequency of 440 Hz. Our perception of frequency is termed pitch. Most sounds are more complicated than a pure tone. For example, a sound made by a musical instrument contains a fundamental frequency and harmonics. The fundamental is the basic frequency, and the harmonics are multiples of the fundamental. For example, if the fundamental is 440 Hz, the harmonics are 880 Hz, 1,320 Hz, 1,760 Hz, and so on. When different instruments play the same note, the notes differ in the relative intensities of the various harmonics and there are subtle qualitative differences between instruments in the way they commence, shape, and sustain the sound; these differences are what give each instrument its characteristic voice, or timbre.
Watson/Breedlove The Mind's Machine Foundations of Brain and Behavior 4e
pinna The external part of the ear. ear canal Also called auditory canal. The tube leading from the pinna to the tympanic membrane. inner ear The cochlea and vestibular apparatus. middle ear The cavity between the tympanic membrane and the cochlea. tympanic membrane Also called eardrum. The partition between the external ear and the middle ear. ossicles Three small bones (incus, malleus, and stapes) that transmit vibration across the middle ear, from the tympanic membrane to the oval window. oval window The opening from the middle ear to the inner ear. cochlea A snail-shaped structure in the inner ear canal that contains the primary receptor cells for hearing. scala vestibuli Also called vestibular canal. One of three principal canals running along the length of the cochlea. scala media Also called middle canal. The central of the three spiraling canals inside the cochlea, situated between the vestibular canal and the tympanic canal. A Touching Moment Helen Keller, who was both blind and deaf, said, "Blindness deprives you of contact with things; deafness deprives you of contact with people"--a poignant reminder of the importance of speech for our social lives. Here, Keller (center, accompanied by her aide and interpreter, Polly Thompson) communicates with U.S. President Dwight Eisenhower by feeling Eisenhower's face as he speaks and makes facial expressions. Rather than living in sensory and social isolation, Keller honed her intact senses to such a degree that she was able to become a noted teacher and writer.
organs; in fact, one of the main jobs of your powers of attention is to filter out the constant barrage of unimportant little noises that your ears detect (see Chapter 14). The external ear captures, focuses, and filters sound The oddly shaped fleshy objects that most people call ears are properly known as pinnae (singular pinna). Aside from their occasional utility as handles and jewelry hangers, the pinnae funnel sound waves into the second part of the external ear: the ear canal (or auditory canal). The pinna is a distinctly mammalian characteristic, and mammals show a wide array of ear shapes and sizes. Furthermore, although only a minority of humans can move their ears--and even then only enough to entertain children--many other mammals deftly shape and swivel their pinnae to help locate the source of a sound. Animals with exceptional auditory localization abilities, such as bats, may have especially mobile ears. The "ridges and valleys" of the pinna modify the character of sound that reaches the middle ear. Some frequencies of sound are enhanced; others are suppressed. For example, the shape of the human ear especially increases the reception of sounds between 2,000 and 5,000 Hz--a frequency range that is important for speech perception. The shape of the external ear--and, in many species, the direction in which it is being pointed--provides additional cues about the direction and distance of the source of a sound, as we will discuss later in this chapter. The middle ear concentrates sound energies A collection of tiny structures made of membrane, muscle, and bone--essentially a tiny biological microphone--links the ear canal to the neural receptor cells of the inner ear (FIGURE 6.1A). This middle ear (FIGURE 6.1B) consists of the taut tympanic membrane (eardrum) sealing the end of the ear canal plus a chain of tiny bones, called ossicles, that mechanically couple the tympanic membrane to the inner ear at a specialized patch of membrane called the oval window. These ossicles, the smallest bones in the body, are called the malleus (Latin for "hammer"), the incus (Latin for "anvil"), and the stapes (Latin for "stirrup"). Sound waves in the air strike the tympanic membrane and cause it to vibrate with the same frequency as the sound; as a result, the ossicles start moving too. Because of how they are attached to the eardrum, the ossicles concentrate and amplify the vibrations, focusing the pressures collected from the relatively large tympanic membrane onto the small oval window. This amplification is crucial for converting vibrations in air into movements of fluid in the inner ear, as we'll see shortly. The middle ear is equipped with the equivalent of a volume control, which helps protect against the damaging forces of extremely loud noises. Two tiny muscles--the tensor tympani and the stapedius (see Figure 6.1B)--attach to the ends of the chain of ossicles. Within 200 milliseconds of the arrival of a loud sound, the brain signals the muscles to contract, which stiffens the chain of ossicles and reduces the effectiveness of the sounds. Interestingly, the middle-ear muscles activate just before we produce self-made sounds like speech or coughing, which is why we don't perceive our own sounds as distractingly loud. The cochlea converts vibrational energy into neural activity The part of the inner ear that ultimately converts vibrations from sound into neural activity--the coiled, fluid-filled cochlea (from the Greek kochlos, "snail")--is a marvel of miniaturization (FIGURES 6.1C and D). In an adult human, the cochlea measures only about 9 millimeters in diameter at its widest point--roughly the size of a pea. Fully unrolled, the human cochlea would be about 35-40 millimeters long. The cochlea is a spiral of three parallel canals: (1) the scala vestibuli (also called the vestibular canal), (2) the scala media (middle canal), and (3) the scala tympani (tympanic canal). The scala media contains the receptor system, called the organ of Corti, that converts vibration (from sound) into neural activity (see Figure 6.1D). It consists
Hearing, Balance, Taste, and Smell 181 FIGURE 6.1 External and Internal Structures of the Human Ear
External ear (pinna) Middle ear Ossicles Ear canal
(B) Middle ear Tensor tympani muscle Ossicles: Malleus Incus Stapes
Outer hair cells Inner hair cell Nerve bers Basilar membrane
Scala vestibuli (vestibular canal) (C) Cochlea
of three main structures: (1) the auditory sensory cells, called hair cells (FIGURE 6.1E), which bridge between the basilar membrane and the overlying tectorial membrane; W(2a)tsaonn/eBlraebeodlroavtee framework of supporting cells; and (3) the auditory nerve terminals TthheaMt tirnadn'ssMmaitchnineeural signals to and from the brain. FoundWatihonesnofthBreaionsasnidclBeeshatvriaorn4semit vibrations from the tympanic membrane to the oval MwMin4de_o0w6.,0w1 av0e3s/0o3r/r2i0pples are created in the fluid of the scala vestibuli, which in turn cause the basilar membrane to ripple, like shaking out a rug. A crucial feature of the basilar membrane is that it is tapered--it's much wider at the apex of the cochlea than at the base. Thanks to this taper, each successive location along the basilar membrane shows its strongest response to a different frequency of sound. High frequencies have their greatest effects near the base, where the basilar membrane is narrow and com- paratively stiff; low-frequency sounds produce a larger response near the apex, where the basilar membrane is wider and floppier, as we'll see next. (Yoon et al., 2011).
scala tympani Also called tympanic canal. One of three principal canals running along the length of the cochlea. organ of Corti A structure in the inner ear that lies on the basilar membrane of the cochlea and contains the hair cells and terminations of the auditory nerve. hair cell One of the receptor cells for hearing in the cochlea, named for the stereocilia that protrude from the top of the cell and transduce vibrational energy in the cochlea into neural activity. basilar membrane A membrane in the cochlea that contains the principal structures involved in auditory transduction. tectorial membrane A gelatinous membrane located atop the organ of Corti.
RESEARCHERS AT WORK Georg von Békésy and the cochlear wave The discovery of the mechanics of the basilar membrane garnered a Nobel Prize for Georg von Békésy in 1961 (FIGURE 6.2).
FIGURE 6.2 Deformation of the Basilar Membrane Encodes Sound Frequencies
Hypothesis That sound waves of different frequencies cause ripples at different places on the basilar membrane.
I. Open a human cochlea (from a cadaver) and add a reflective fluid.
II. Bounce intense flash of light off the basilar membrane during vibration at the oval window.
1 High frequencies displace basilar membrane in base of cochlea. Cochlear base
"Unrolling" of cochlea 2 Low frequencies displace basilar membrane in apex of cochlea. Cochlear apex
4 ...and recorded by a camera to measure membrane displacement at different frequencies.
3 A flash of intense light is bounced off the basilar membrane...
Result "Standing waves" are observed on the basilar membrane, their position corresponding to frequency of the vibration.
These experiments revealed an orderly map of frequencies along the tapering length of the basilar membrane, from low frequencies at the broad and floppy apex to high frequencies at the stiff and narrow base.
That the frequency of a sound is encoded by the specific location on the basilar membrane that shows the largest displacement in response to the sound. High frequencies displace the basilar membrane at the base of the cochlea; low frequencies cause displacement at the apex. This differential response depending on
location along the membrane has become known as place coding.
The hair cells transduce movements of the basilar membrane into electrical signals
The rippling of the basilar membrane is converted into neural activity through the ac- stereocilium A tiny bristle that
tions of the hair cells. Each hair cell features a sloping brush of minuscule hairs called stereocilia (singular stereocilium) on its upper surface. In Figure 6.1D you'll notice that,
protrudes from a hair cell in the auditory or vestibular system.
although the bases of hair cells are implanted in the basilar membrane, the stereocilia nestle into hollows in the tectorial membrane that lies above. The hair cells--and especially the stereocilia themselves--thus form a mechanical bridge between the two membranes that is forced to bend when sounds cause the basilar membrane to ripple.
inner hair cell (IHC) One of the two types of receptor cells for hearing in the cochlea. Compared with outer hair cells, IHCs are positioned closer to the central axis of the coiled cochlea.
Even a tiny bend of the stereocilia produces a large and rapid depolarization of the hair cells. This depolarization results from the operation of a special type of large
outer hair cell (OHC) One of the two types of receptor cells for hearing in the
and nonselective ion channel found on stereocilia. Like spring-loaded trapdoors, these
channels are mechanically popped open as stereocilia bend (Hudspeth et al., 2000), allowing an inrush of potassium (K+) and calcium (Ca2+) ions. Just as we saw in neu-
OHCs are positioned farther from the central axis of the coiled cochlea.
rons (in Chapter 2), this depolarization leads to a rapid influx of Ca2+ at the base of the hair cell, which in turn causes synaptic vesicles there to fuse with the presynaptic membrane and release neurotransmitter, stimulating adjacent nerve fibers. The ste-
vestibulocochlear nerve Cranial nerve VIII, which runs from the cochlea to the brainstem auditory nuclei.
reocilia channels snap shut again in a fraction of a millisecond as the hair cell sways
back. This ability to rapidly switch on and off allows hair cells to accurately track the
rapid oscillations of the basilar membrane with exquisite sensitivity.
In the human cochlea, the hair cells are organized into a single row of about 3,500
inner hair cells (IHCs, called inner because they are closer to the central axis of the
coiled cochlea) and about 12,000 outer hair cells (OHCs) in three rows (see Figure
6.1D). Fibers of the vestibulocochlear nerve (cranial nerve VIII) contact the bases of
the hair cells (see Figure 6.1E). Some of these
fibers do indeed convey sound information to
the brain, but the neural connections of the cochlea are a little more complicated than this. In
The outer and inner hair cells form synaptic connections to and from the brain.
fact, there are four kinds of neural connections with hair cells, each relying on a different neurotransmitter (Goutman et al., 2015), as you can
1. IHC afferents convey to the brain the action potentials that provide the perception of
2. IHC efferents lead from the brain to the IHCs. They allow the brain to control the responsiveness of IHCs. 3. OHC afferents convey information to the brain about the mechanical state of the basilar membrane, but not the perception of sounds themselves. 4. OHC efferents from the brain enable it to activate a remarkable property of OHCs, making them change their length almost instantaneously (Zheng et al., 2000; He et al., 2014). Through this electromechanical action, the brain continually modifies the stiffness of regions of the basilar membrane, resulting in both sharpened tuning and pronounced amplification (Hudspeth, 2014). Evidence is mounting
(B) Outer hair cell Acetylcholine (ACh) GABA
Different synaptic transmitters are hypothesized to be active at the synapses of inner and outer hair cells in the organ of Corti.
3. OHC afferent, to brain 4. OHC efferent, from brain
FIGURE 6.3 Auditory Nerve Fibers and Synapses in the Organ of Corti
that a complementary process also modifies the local stiffness of the tectorial membrane (see Figure 6.3A), further improving the tuning and amplification of the organ of Corti (Sellon et al., 2019). Now that the inner ear has transduced the vibrations from sound into trains of action potentials, the auditory signals must leave the cochlea and enter the brain.
Auditory signals run from cochlea to cortex
On each side of your head, about 30,000-50,000 audito-
ry axons from the cochlea make up the auditory part of the
vestibulocochlear nerve (cranial nerve VIII), and most of
these afferent fibers carry information from the IHCs (each
of which stimulates several nerve fibers) to the brain. If we
record from these IHC afferents, we find that each one has a
maximum sensitivity to sound of a particular frequency but
will also respond to neighboring frequencies if the sound is
50 loud enough. For example, the auditory neuron whose re-
sponses are shown in red in FIGURE 6.4 has its best frequen-
FIGURE 6.4 Tuning Curves of Auditory Nerve Cells (After N. Y.-S. Kiang et al., 1965. Discharge patterns of single fibers in the cat's auditory nerve. MIT Press. Cambridge, MA.)
cy at 1,200 Hz (1.2 kHz)--that is, it is sensitive to even a very weak tone at 1,200 Hz--but for sounds that are 20 dB louder, the cell will respond to frequencies from 500 to 1,800 Hz. We call this the cell's tuning curve. If the brain received a signal
Watson/Breedlove The Mind's Machine FcooucndhalteioanrsnofuBcrlaeinianBdrBaeinhsavteiomr 4neuclei that receive input from auditory hair cells and MseMnd4eo_u06tp.0u4t to0t3h/e02s/u2p0erior olivary nuclei.
from only one such fiber, it would not be able to tell whether the stimulus was a weak tone of 1,200 Hz or a stronger tone of 500 or 1,800 Hz, or any frequency in between. Instead, the brain analyzes the activity from thousands of such units simultaneously to calculate the intensity and frequency of each sound.
The inputs from the auditory nerves are distributed to both sides of the brain
via the ascending network shown in FIGURE 6.5. First, the auditory nerve
fibers terminate in the (sensibly named) cochlear nuclei, where some
initial processing occurs. Output from the cochlear nuclei primarily
Brainstem FIGURE 6.5 Auditory Pathways of the Human Brain Watson/Breedlove
Auditory cortex Medial geniculate nucleus Inferior colliculus Superior olivary nucleus Cochlear nucleus Cochlea L R Binaural (two-ear) interactions commence in the brainstem superior olivary nucleus. Most (but not all) of the information from each ear projects to the cortex on the opposite side of the brain, depicted by the blended colors in this schematic.
projects to the superior olivary nuclei, each of which receives inputs from both right and left cochlear nuclei. This bilateral input makes the superior olivary nucleus the first brain site at which binaural (two-ear) processing occurs. As you might expect, this mechanism plays a key role in localizing sounds by comparing the two ears, as we'll discuss shortly. The superior olivary nuclei pass information derived from both ears to the inferior colliculi, which are the primary auditory centers of the midbrain. Outputs of the inferior colliculi go to the medial geniculate nuclei of the thalamus. Outputs from the medial geniculate nuclei extend to several auditory cortical areas. The neurons within all levels of the auditory system, from cochlea to auditory cortex, display tonotopic organization; that is, they are internally arranged according to an orderly map of sound frequencies (topos is Greek for "place") from low frequency (sounds that we perceive as lower pitched or "bass") to high frequency (perceived as higher pitched or "treble"). Furthermore, at the higher levels of the auditory system, auditory neurons are not only excited by specific frequencies, but also inhibited by neighboring frequencies, resulting in much sharper tuning of the frequency responses of these cells. This precision helps us discriminate tiny differences in the frequencies of sounds. Brain-imaging studies in humans confirm that many sounds (tones, noises, and so on) activate the primary auditory cortex (A1), which is located on the upper surface of the temporal lobes (FIGURE 6.6A). Speech sounds produce similar activation, but they also activate other, more specialized auditory areas (FIGURE 6.6B). Interestingly, at least some of these regions are activated in hearing people when they try to lip-read-- that is, to understand someone by watching that person's lips without auditory cues (Calvert et al., 1997; L. E. Bernstein et al., 2002). This suggests that the auditory cortex integrates other, nonauditory, information with sounds. (The organization of auditory cortical areas in other species is described in A STEP FURTHER 6.1, on the website.)
superior olivary nuclei Brainstem nuclei that receive input from both right and left cochlear nuclei and provide the first binaural analysis of auditory information. inferior colliculi Paired gray matter structures of the dorsal midbrain that process auditory information. medial geniculate nucleus Either of two nuclei--left and right--in the thalamus that receive input from the inferior colliculi and send output to the auditory cortex. tonotopic organization The organization of auditory neurons according to an orderly map of stimulus frequency, from low to high. primary auditory cortex Also called A1. The cortical region, located on the superior surface of the temporal lobe, that processes complex sounds transmitted from lower auditory pathways. View Animation 6.4: Mapping Auditory Frequencies
Functional-MRI scans show that pure tones or noise activate chie y the primary auditory area of the temporal lobe...
...while speech sounds activate other auditory cortical regions, as well as the primary auditory area. R
From J. R. Binder et al., 1994. Ann. Neurol. 35: 662, courtesy of Jeffrey Binder
From M. I. Posner and M. E. Raichle, 1994. Images of mind. Scientific American Library. New York, NY, courtesy of Marcus Raichle
PET scans show that listening to words activates not only several regions of the cerebral cortex, but also regions of the thalamus and the cerebellum. The numbered horizontal lines in the left panel correspond to the levels of the horizontal sections in the panel at right.
FIGURE 6.6 Responses of the Human Auditory Cortex to Random Sounds versus Speech
1. Identify the major components of the external ear. What does the external ear do? 2. Identify the three ossicles, and explain their function. To what structures do the ossicles connect, and how is their action moderated? 3. Provide a brief description of the organ of Corti, naming the components that are most important for the perception of sound. 4. Explain how the movement of hair cells transduces sound waves into action potentials. Compare and contrast the functions of inner hair cells and outer hair cells. 5. Sketch the major anatomical components of the auditory projections in the brain. Where does binaural processing first occur? What is tonotopic organization? What kind of processing does auditory cortex perform?
place coding theory Theory that the pitch of a sound is determined by the location of activated hair cells along the length of the basilar membrane.
6.2Specialized Neural Systems Extract Information from Auditory Signals Higher levels of the auditory system process different features of the sounds captured by the ears. After reading this section, you should be able to: 6.2.1 Explain the relationship between frequency and pitch, and discuss the ranges of frequencies perceived by humans and other species. 6.2.2 Describe the two major ways in which frequency information is encoded. 6.2.3 Explain the principal features of sound that the nervous system uses for sound localization. 6.2.4 Discuss the functions of auditory cortex, from an ecological perspective. 6.2.5 Evaluate the importance of experience in the development and tuning of the auditory system, throughout the life span. 6.2.6 Describe the relationship between musical experience and the development of auditory competencies in music and other domains. At least when we're young, most of us can hear sounds ranging from 20 Hz to about 20,000 Hz, and within this range we can distinguish between sounds that differ by just a few hertz. Our ability to discern many frequencies simultaneously, and accurately identify where in the world they are coming from, helps us to define the spaces and sound emitters around us--acoustical objects as varied as insects and tubas--and identify the ones that are important for our daily lives. The pitch of sounds is encoded in two complementary ways Differences in frequency are important for our sense of pitch, but pitch and frequency are not synonymous. Frequency describes a physical property of sounds (see Box 6.1), but pitch relates solely to our subjective perception of those sounds. This is an important distinction because frequency is not the sole determinant of perceived pitch; at some frequencies, higher-intensity sounds may seem higher pitched, and changes in pitch do not precisely parallel changes in frequency. How do we distinguish pitches? Two signals from the cochlea appear to inform the brain about the pitch of sounds: 1. According to place coding theory, the pitch of a sound is determined by the location of activated hair cells along the length of the basilar membrane, as we discussed in this chapter's Researchers at Work feature. So, activation of receptors near the base of the cochlea (which is narrow and stiff and responds to high frequencies) signals treble, and activation of receptors nearer the apex (which is wide and floppy and responds to low frequencies) signals bass. This is another example of the labeled
lines we discussed in Chapter 5--each neuron fires in response to its particular favorite frequency. 2. A complementary account called temporal coding theory proposes that the frequency of auditory stimuli is encoded in the rate of firing of auditory neurons. According to this model, the frequency of action potentials produced by the neuron is directly mathematically related to the number of cycles per second (i.e., hertz) of the sound. For example, a 500 Hz sound might cause some auditory neurons to fire 500 action potentials per second. Encoding sound frequency within volleys of action potentials averaged across a number of neurons with similar tunings provides the brain with a reliable additional source of pitch information. Experimental evidence indicates that we rely on both of these processes to discriminate the pitch of sounds. Temporal coding is most evident at lower frequencies, up to about 4,000 Hz: auditory neurons can fire a maximum of only about 1,000 action potentials per second, but to some extent they can encode sound frequencies that are multiples of the action potential frequency. Beyond about 4,000 Hz, however, this encoding becomes impossible, and pitch discrimination relies on place coding of pitch along the basilar membrane. Mammalian species employ a huge range of frequencies in their vocalizations, from infrasound (less than 20 Hz) in elephants and whales to ultrasound (greater than 20,000 Hz) in bats and porpoises and many other species (the ghost-faced bat emits vocalizations at an incredible 160,000 Hz). These sounds have been shaped by evolution to serve special purposes. For example, many species of bats analyze the reflected echoes of their ultrasonic vocalizations to navigate and hunt in the dark. At the other end of the spectrum, elephants emit ultra-low-frequency alarm calls that are so powerful that they travel partly through the ground and are detected seismically by other elephants (O'Connell-Rodwell, 2007; Herbst et al., 2012) and yet are so nuanced that the elephants can distinguish human-related threats from bee-related threats (Soltis et al., 2014) and can use their "rumbles" to identify potential mates (Stoeger and Baotic, 2017). Brainstem systems compare the ears to localize sounds Being able to quickly identify where a sound is coming from--whether it is the crack of a twig under a predator's foot, or the sweet tones of a would-be mate--is a matter of great evolutionary significance. So it's no surprise that we are remarkably good at locating a sound source (our accuracy is about ±1 degree horizontally around the head, and many animals do even better). The auditory system accomplishes this feat by analyzing two kinds of binaural cues that signal the location of a sound source: 1. Interaural intensity differences (IIDs) result from comparison of the intensity of the sound--the physical property that we perceive as loudness--at the left and right ears (interaural means"between the two ears"). Depending on the species-- and the placement and characteristics of their pinnae--intensity differences occur because one ear is pointed more directly toward the sound source or because the head casts a sound shadow (FIGURE 6.7A), preventing sounds originating on one side (called off-axis sounds) from reaching both ears with equal loudness. The head shadow (or sound shadow) effect is most pronounced for higher-frequency sounds (FIGURE 6.7B). 2. Interaural temporal differences (ITDs) are differences between the two ears in the time of arrival of sounds. They arise because one ear is always a little closer to an off-axis sound than the other ear is. Two kinds of temporal (time) differences are present in a sound: onset disparity, which is the difference between the two ears in hearing the beginning of the sound; and ongoing phase disparity, which is the continuing mismatch between the two ears in the time of arrival of all the peaks and troughs that make up the sound wave, as illustrated in FIGURE 6.7C.
temporal coding theory Theory that the pitch of a sound is determined by the rate of firing of auditory neurons. infrasound Very-low-frequency sound, generally below the 20 Hz threshold for human hearing. ultrasound Very-high-frequency sound, generally beyond 20,000 Hz, which is the upper bound for a young adult human. interaural intensity difference (IID) A perceived difference in loudness between the two ears, which the nervous system can use to localize a sound source. interaural temporal difference (ITD) A difference between the two ears in the time of arrival of a sound, which the nervous system can use to localize a sound source.
The two ears receive different information from each side of the observer's midline, accentuated by the head's sound shadow. Sound shadow
Differences in perceived intensity are greater at higher frequencies. (B) L
Sounds take longer to reach the more distant ear, resulting in binaural differences in time of arrival.
FIGURE 6.7 Cues for Binaural Hearing
Onset disparity is the latency difference between the two ears for the beginning of a sound.
Ongoing phase disparity is the difference between the ears for arrival of the peaks and troughs of the sound wave.
Watson/Breedlove The Mind's Machine Foundations of Brain and Behavior 4e MM4e_06.07 03/02/20 spectral filtering The process by which the hills and valleys of the external ear alter the amplitude of some, but not all, frequencies in a sound.
Both types of cues are employed in sound localization. At low frequencies, though, no matter where sounds are presented horizontally around the head, there are virtually no intensity differences between the ears. For these frequencies, differences in times of arrival are the principal cues for sound localization (and at very low frequencies, neither cue is much help; this is why you can place the subwoofer of an audio system anywhere you want within a room). At higher frequencies, however, the sound shadow cast by the head produces significant binaural intensity differences. Of course, we can't perceive which types of processing we're relying on for any given sound; in general, we are aware of the results of neural processing but not the processing itself. (You can learn about brain mechanisms of auditory localization in A STEP FURTHER 6.2, on the website.) The structure of the external ear provides yet another localization cue. As we mentioned earlier, the hills and valleys of the external ear selectively reinforce some frequencies in a complex sound and diminish others. This process is known as spectral filtering, and the frequencies that are affected depend on the angle at which the sound arrives at those peaks and valleys (Kulkarni and Colburn, 1998; Zonooz et al., 2019). That angle varies, of course, depending on where the sound comes from; these spectral cues provide critical information about the vertical localization (or elevation) of a sound source. Without them, you would have a hard time knowing whether a sound from straight in front of you came from the ground or from the treetops. The various binaural and spectral cues used for sound localization converge and are integrated in the inferior colliculus (Slee and Young, 2014). The auditory cortex processes complex sound In some sensory areas of the brain, lesions cause the loss of basic perceptions. For example, lesions of visual cortex result in blind spots, as we will discuss in Chapter 7. But the auditory cortex is different: researchers have long known that simple pure tones can be heard even after the entire auditory cortex has been surgically removed (Neff and Casseday, 1977). So if the auditory cortex is not involved in basic auditory perception, then what does it do? The auditory cortex seems to be specialized for the
detection of more-complex "biologically relevant" sounds, of the sort we mentioned earlier--vocalizations of animals, footsteps, snaps, crackles, and pops--containing many frequencies and complex patterns (Theunissen and Elie, 2014). In other words,
Before training, the "best frequency" of this auditory cortical cell of an adult guinea pig was about 0.7 kilohertz (kHz).
Conditioned-stimulus frequency used for training
After training with a 2.5 kHz tone, the best frequency of this same neuron shifted to 2.5 kHz.
the auditory cortex evolved to process the sounds of
The unique capabilities of the auditory cortex
result from a sensitivity that is fine-tuned by expe-
rience as we grow (Kandler et al., 2009). Human in-
fants have diverse hearing capabilities at birth, but
their hearing for complex speech sounds in partic-
ular becomes more precise and rapid through expo-
sure to the speech of their families and other people.
Newborns can distinguish all the different sounds
that are made in any human language. But as they
develop, they get better and better at distinguishing
sounds in the language(s) they hear, and worse at
distinguishing sounds that occur in other languag-
es. Similarly, early experience with binaural hearing,
compared with equivalent monaural (one-eared)
hearing, has a significant effect on the ability of
children to localize sound sources later in life (W. D. Beggs and Foreman, 1980). Studies with lab animals
FIGURE 6.8 Long-Term Retention of a Trained Shift in the Tuning of an Auditory Receptive Field (After N. M. Weinberger, 1998. Neurobiol.
confirm that experience with sounds of a particular
frequency can cause a rapid retuning of auditory
neurons (FIGURE 6.8; N. M. Weinberger, 1998; Fritz Watson/Breedlove et al., 2003). (You can learn about the role of experienceThine Mauinddi'tsoMryaclhoincealization in owls in A STEP FURTHER 6.3, on the website). Later inFliofuen,daagtioinsgotfaBkraeisn ansdteBaehdayvitoor l4le
on our hearing, gradually impairing auditory cortex neurons and reducing our ability MM4e_06.08 04/16/20 to distinguish between sounds that occur simultaneously (Overton and Recanzone,
2016; Recanzone, 2018). So it turns out there's a good reason why grandparents find it
so difficult to follow a conversation in a noisy restaurant.
Music also shapes the responses of auditory cortex. It might not surprise you to
learn that the auditory cortex of trained musicians shows a bigger response to mu-
sical sounds than does the same cortex in nonmusicians. After all, when two people
differ in any skill, their brains must be different in some way, and maybe people
born with brains that are more responsive to complex sounds are also more likely to
become musicians. The surprising part is that the extent to which a musician's brain
is extra sensitive to musical notes is correlated with the age at which they began their
serious training in music: the earlier the training began, the bigger the difference in
auditory cortex in adulthood (Pantev et al., 1998). Kids who receive intensive musical
education also show enhanced speech perception later in life (Weiss and Bidelman,
2015; Intartaglia et al., 2017). Findings like these show that early musical training
alters the functioning of auditory cortex later in an enduring manner. By adulthood,
the portion of primary auditory cortex where music is first processed, called Heschl's
gyrus, is more than twice as large in professional musicians as in nonmusicians, and
more than twice as strongly activated by music (P. Schneider et al., 2002). And in
addition to the effects of early musical experience on auditory structures, cortical re-
gions that process music are reportedly influenced by the brain's mesolimbic reward
system (see Chapter 3) to attach a reward value to music that is new to us (Salimpoor
So, to what extent is music perception inborn? Some people show a lifelong inability to discern tunes or sing, called amusia. Amusia is associated with subtly abnormal
amusia A disorder characterized by the inability to discern tunes accurately
function in the right frontal lobe and impoverished connectivity between frontal and or to sing.
Diffusion tensor imaging (DTI) of axon projections reveals the arcuate fasciculus (yellow), a pathway connecting the frontal cortex, which is active during pitch discrimination, to the temporal lobe, where auditory processing begins (arrows).
From P. Loui et al. 2009. J. Neurosci. 29: 10215. © 2009 Society for Neuroscience
The arcuate fasciculus is much more prominent in these four control cases...
...than in these four people with amusia.
FIGURE 6.9 Brain Connections in People with Amusia
temporal cortex (FIGURE 6.9) (K. L. Hyde et al., 2006; Loui et al., 2009). The result is an inability to consciously access pitch information, even though cortical pitch-processing systems are intact (Zendel et al., 2015). Interestingly, studies of people with amusia indicate that when listening to music, we process pitch and rhythm quite separately (K. L. Hyde and Peretz, 2004). If you're worried about your own ability to carry a tune, the National Institutes of Health (NIH) provides an online test of pitch perception at www.nidcd.nih.gov/tunestest/test-your-sense-pitch.
Watson/Breedlove The Mind's Machine Foundations of Brain and Behavior 4e MM4e_04.09 06/03/20
Next we consider the main causes of auditory dysfunction. After reading this section, you should be able to: 6.3.1 Define and distinguish between hearing loss and deafness. 6.3.2 Describe and contrast the three major categories of hearing loss. 6.3.3 Identify potentially harmful noise intensities, and discuss the ways in which noise damages the auditory system. 6.3.4 Summarize and evaluate methods for treating each form of hearing loss.
hearing loss Decreased sensitivity to sound, in varying degrees. deafness Hearing loss so profound that speech perception is lost. conduction deafness A hearing impairment in which the ears fail to convert sound vibrations in air into waves of fluid in the cochlea. It is associated with defects of the external ear or middle ear.
Disorders of hearing, including hearing loss (defined as a moderate to severe decrease in sensitivity to sound) and deafness (defined as hearing loss so profound that speech cannot be perceived even with the use of hearing aids), affect about 15% of the population: some 37.5 million people in the United States alone (Blackwell et al., 2014). By now, you may have anticipated that there are three kinds of problems that can prevent sound waves in the air from being transformed into conscious auditory perceptions: problems with sound waves reaching the cochlea, trouble converting sound waves into action potentials, and dysfunction of brain regions that process sound (FIGURE 6.10): 1. Before anything even happens in the nervous system, the ear may fail to convert the sound vibrations in air into waves of fluid within the cochlea. This form of hearing loss, called conduction deafness (FIGURE 6.10A), often comes about when the ossicles of the middle ear become fused together and vibrations of the eardrum can no longer be conveyed to the oval window of the cochlea.
Conduction deafness usually involves a middle ear problem that blocks sound vibrations from reaching the inner ear. (A)
In sensorineural deafness, there is a problem with the structures-- especially the cochlea--that convert sound vibrations into neural activity and project to the brain. (B)
In central deafness, damage to auditory brain structures can affect hearing in various ways. (C)
Micrographs by H. Engstrom and B. Engstrom, courtesy of Widex
FIGURE 6.10 Types of Hearing Loss
2. Even if vibrations are successfully conducted to the cochlea, the sensory apparatus Watsonf/thBreeecdolcohvleea--the organ of Corti, and the hair cells it contains--may fail to convert The Mthinedr'ispMpalecshicnreeated in the basilar membrane into the volleys of action potentials that Foundations of Brain and Behavior 4e ordinarily inform the brain about sounds. This form of hearing loss, termed sensoMM4rein_0e6u.1r0al d0e3a/0fn3/e2s0s (FIGURE 6.10B), is most often the result of permanent damage or destruction of hair cells by any of a variety of causes (FIGURE 6.11). Some people
sensorineural deafness A hearing impairment most often caused by the permanent damage or destruction of hair cells or by interruption of the vestibulocochlear nerve that carries auditory information to the brain.
In a normal cochlea, hair cells line the organ of Corti throughout its length, but exposure to excessively loud sounds can have rapid destructive effects. After exposure to excessive noise, a long section of the sound-damaged cochlea is completely missing its hair cells, resulting in deafness from the corresponding frequencies.
Electron microscopy reveals that the orderly rows of stereocilia found in the organ of Corti in a normal cochlea are crushed and attened by excessive noise exposure, like trees blown down in a windstorm.
FIGURE 6.11 The Destructive Effects of Loud Noise
FIGURE 6.12 How Loud Is Too Loud? 140 Jet engine
Because the decibel scale is logarithmic, a noise that is 10 dB greater is actually 100 times louder.
130 Firing a gun 120 Jackhammer 110 Concert venue/club 100 Loud music via headphones 90 Motorcycle
Extended exposure to sounds over 90 dB may be harmful. As little as 30 minutes of exposure to sounds over 110 dB can harm hearing.
80 City traf c 70 Vacuum cleaner Normal 60 conversation 50 Leaves rustling Decibels
tinnitus A sensation of noises or ringing in the ears not caused by external sound. central deafness A hearing impairment in which the auditory areas of the brain fail to process and interpret action potentials fromWsoatusnodn/sBtirmeeudliloinvemeaningful ways, usuaTllhyeaMs iandc'osnMseacqhuiennece of damage in audiFtooruyndbartaioinnsaorfeBarsa.in and Behavior 4e wordMdMe4aef_n0e6.s1s2 A06f/o2r5m/2o0f central deafness that is characterized by the specific inability to hear words although other sounds can be detected. cortical deafness A form of central deafness, caused by damage to both sides of the auditory cortex, that is characterized by difficulty in recognizing all complex sounds, whether verbal or nonverbal.
Possible hearing loss in as little as 30 minutes.
are born with genetic abnormalities that interfere with the function of hair cells (Petit and Richardson, 2009). Many more people acquire sensorineural deafness during their lives as a result of being exposed to extremely loud sounds--overamplified music, nearby gunshots, and industrial noise are important examples--or because of medical problems such as infections and adverse drug effects (certain antibiotics, such as streptomycin, are particularly ototoxic). If you don't think it can happen to you, think again. Anyone listening to something for more than 5 hours per week at 89 dB or louder is already exceeding workplace limits for hearing safety (SCENIHR, 2008), yet many personal music players and music at concerts and clubs exceed 100 dB. Fortunately, earplugs are available that attenuate all frequencies equally, making concerts a little quieter without muffling the music.Various sound sources are compared in FIGURE 6.12; if you are concerned about your own exposure, excellent sound level meter apps for smartphones are available at little or no cost (including one from the National Institute for Occupational Safety and Health (NIOSH) at www.cdc.gov/niosh/topics/noise/app. html). Long-term exposure to loud sounds can cause lasting hearing problems ranging from a persistent ringing in the ears, called tinnitus (Zenner et al., 2017), to a permanent profound loss of hearing for the frequencies being listened to at such high volumes.
3. For the action potentials sent from the cochlea to be of any use, the auditory areas of the brain must process and interpret them in meaningful ways. Central deafness (FIGURE 6.10C) occurs when auditory brain areas are damaged by, for example, strokes, tumors, or traumatic injuries. As you might expect from our earlier discussion of auditory processing in the brain, this type of deafness almost never involves a simple loss of auditory sensitivity. Afflicted individuals can often hear a normal range of pure tones but are impaired in the perception of complex, behaviorally relevant sounds. An example in humans is word deafness: selective trouble with speech sounds despite normal speech and normal hearing for nonverbal sounds. In cortical deafness--a rare syndrome involving bilateral lesions of auditory cortex--patients have more-complete impairment, struggling to recognize all complex sounds, whether verbal or nonverbal.
Although there are few treatments available for central deafness, we can use electronic prostheses to restore the auditory stimulation that is missing in conduction or sensorineural deafness. We discuss these approaches in Signs & Symptoms, next.
SIGNS & SYMPTOMS (A) Skin Transmitter Microphone (rests behind ear)
Scala vestibuli Vestibular Scala media Scala tympani (vestibular canal) membrane (middle canal) (tympanic canal)
(B) FIGURE 6.13 Cochlear Implants Provide Hearing in Some Deaf People
From G. Clark. 2003. Cochlear Implants: Fundamentals and Applications. Springer Nature: New York. Reprinted by permission.
Restoring Auditory Stimulation in Deafness
People with conduction deafness use hearing aids that employ electronic amplification to deliver louder sounds to the impaired--but still functional--auditory system, and it is sometimes possible to surgically free up the fused ossicles or replace them with Teflon prosthetics and thus restore the transmission of sound vibrations to the cochlea. But sensorineural deafness presents a much thornier problem because neural elements have been destroyed (or were absent from birth). Can new hair cells be grown? Although fishes and amphibians produce new hair cells throughout life, mammals traditionally have long been viewed as incapable of regenerating hair cells. This conclusion may have been too hasty, however (Géléoc and Holt, 2014). Using several different strategies, researchers have succeeded in inducing the birth of new hair cells in cochlear tissues of lab animals (Li et al., 2015), so there is reason to hope that an effective restorative therapy for deafness may be available someday. For now, treatments for sensorineural deafness focus on the use of prostheses. Implantable devices called cochlear implants can detect sounds and then directly stimulate the auditory nerve fibers of the cochlea, bypassing the ossicles and hair cells altogether and offering partial restoration of hearing even in cases of complete Watson/Breedlove sTehnesoMriinnedu'sraMl adcehainfneess (FIGURE 6.13). You may have had doubts aFboouuntdtahtieonvsaoluf BeroaifnBaénkdéBseyh'asvwioror4ke with cadavers that we described at the start of this chapter. If so, consider this: the cochlear implants that MM4e_06.13 08/31/20 have brought hearing to thousands of deaf people work by reproducing the phenomena Békésy discovered. In other words, the device
sends information about low frequencies to electrodes stimulating nerves at the apex of the cochlea and sends information about high frequencies to electrodes stimulating nerves at the base. As you might predict from our discussion of the importance of experience in shaping auditory responsiveness, the earlier in life these devices are implanted, the better the person will be able to understand complex sounds, especially speech (Geers et al., 2017). So in a sense, the success of these implants is due to the cleverness of the brain. cochlear implant An implantable device that detects sounds and selectively stimulates nerves in different regions of the cochlea.
1. Compare and contrast the two important signals about pitch that the brain receives from the cochlea: place coding and temporal coding. How do they work together to give us our sense of pitch? 2. Discuss the sensory capabilities of different species as adaptations shaped by natural selection. 3. Provide an account of sound localization, identifying the several sources of information that we use to determine the source of a sound. 4. Discuss the types of processing that are performed by primary auditory cortex. Is experience with sound important for development of cortical auditory systems? 5. Name and describe the three major forms of deafness.
6.4Balance: The Inner Ear Senses the Position and Movement of the Head
vestibular system The sensory system that detects balance. It consists of several small inner-ear structures that adjoin the cochlea. semicircular canal Any one of the three fluid-filled tubes in the inner ear that are part of the vestibular system. Each of the tubes, which are at right angles to each other, detects angular acceleration in a particular direction. ampulla An enlarged region of each semicircular canal that contains the receptor cells (hair cells) of the vestibular system.
In the next section we look at the inner ear system that gives us our sense of balance. After reading this section, you should be able to: 6.4.1 Describe the anatomical features of the vestibular system. 6.4.2 Explain how accelerations and changes in the position of the head are transduced into sequences of action potentials. 6.4.3 Describe the vestibular projections to the brainstem, and summarize the functional importance of these projections. 6.4.4 Discuss some of the consequences of vestibular dysfunction or abnormal vestibular stimulation. Without our sense of balance, it would be a challenge to simply stand on two feet. When you use an elevator, you clearly sense that your body is rising or falling, despite the sameness of your surroundings. When you turn your head, take a tight curve in your car, or bounce through the seas in a boat, your continual awareness of motion allows you to plan further movements and anticipate changes in perception due to movement of your head. And of course, too much of this sort of stimulation can make you lose your lunch. Like hearing, our sense of balance is the product of the inner ear, relying on several small structures that adjoin the cochlea and are known collectively as the vestibular system (from the Latin vestibulum, "entrance hall," reflecting the fact that the system lies in hollow spaces in the temporal bone). In fact, it is generally accepted that the auditory organ evolved from the vestibular system, although the ossicles probably evolved from parts of the jaw. The most obvious components of the vestibular system are the three fluid-filled semicircular canals, plus two bulbs called the saccule and the utricle that are located near the ends of the semicircular canals (FIGURE 6.14A). Notice that the three canals are oriented in the three different planes in which the head can rotate (FIGURE 6.14B)--nodding up and down (technically known as pitch), shaking from side to side (yaw), and tilting left or right (roll). The receptors of the vestibular system are hair cells--just like the ones in the cochlea--whose bending ultimately produces action potentials. The cilia of these hair cells are embedded in a gelatinous mass inside an enlarged chamber called the ampulla (plural ampullae) that lies at the base of each semicircular canal (see Figure 6.14B). Movement of the head in one axis sets up a flow of the fluid in the semicircular canal that lies in the same plane, bending the stereocilia in that particular ampulla and signaling the brain that the head has moved. Working together, the three semicircular canals accurately track the movement of the head. The utricle and saccule each contain an otolithic membrane (a gelatinous sheet studded with tiny crystals; otolith literally means "ear stone") that, thanks to its mass, lags slightly when
Hearing, Balance, Taste, and Smell 195 FIGURE 6.14 Structures of the Vestibular System
Yaw The vestibular apparatus, with semicircular canals in each of the three axes of rotation, is attached to the cochlea.
(B) Semicircular canals Head movement Movements of the head involve rotation around the three principal axes.
Vestibular response Each type of head movement is registered by a corresponding semicircular canal in the same plane of rotation. The rotation of the head is translated into movement of gel within the semicircular canals, which stimulates hair cells in ampullae at the base of the canals, exciting the vestibulocochlear nerve.
the head moves. This bends nearby hair cells, stimulating them to track straight-line acceleration and deceleration--the final signals that the brain needs in order to calculate the position and movement of the body in three-dimensional space. Nerve fibers leading from these hair cells to the brain make up the vestibular part of the vestibulocochlear nerve (cranial nerve VIII). Vestibular information is crucial for planning body movements, maintaining balance against gravity, and smoothly directing sensory organs like the eyes and ears toward specific locations, even when our bodies are themselves in motion. So, it's no surprise that the nerve pathways from the vestibular system have strong connections to brain regions responsible for the planning and control of movement. On entering the brainstem, many of the vestibular fibers terminate in the vestibular nuclei, wWhatisloens/oBmreeedlfoibveers project directly to the cerebellum to aid in motor programming tThheerMe.inOdu'stMpuacthsifnreom the vestibular nuclei project in a complex manner to motor areas Foundations of Brain and Behavior 4e tDhrraogounghyoMuetdtihaeGbroruapin, including motor nuclei of the eye muscles, the thalamus, and tMhMe c4e_r0e6b.1ra4l co08r/te31x/. 20
View Animation 6.5: The Vestibular System vestibular nuclei Brainstem nuclei that receive information from the vestibular organs through cranial nerve VIII (the vestibulocochlear nerve).
196CHAPTER6 motion sickness The experience of nausea brought on by unnatural passive movement, as may occur in a car or boat.
Some forms of vestibular excitation produce motion sickness There is one aspect of vestibular activation that many of us would gladly do without. Too much strong vestibular stimulation--think of boats and roller coasters--can produce the misery of motion sickness. Motion sickness is caused by movements of the body that we cannot control. For example, passengers in a car are more likely to suffer from motion sickness than is the driver. Why do we experience motion sickness? According to the sensory conflict theory, we feel bad when we receive contradictory sensory messages, especially a discrepancy between vestibular and visual information. One hypothesis is that the stimulation is activating a system that originally evolved to rid the body of swallowed poison (M. Treisman, 1977). According to this hypothesis, discrepancies in sensory information might normally signal a dangerous neurological problem, triggering dizziness and vomiting to get rid of potentially toxic food. However, there is little objective evidence to support the "poison hypothesis," and overall the evolutionary origins of motion sickness remain a mystery (Oman, 2012). The observation that virtual reality devices frequently induce motion sickness, and that susceptibility to this sickness is associated with individual differences in pre-test body sway, has been interpreted as evidence that motion sickness results from postural instability rather than sensory conflict (Munafo et al., 2017). When an airplane bounces around in turbulence, the vestibular system signals that various changes in direction and accelerations are occurring, but as far as the visual system is concerned, nothing is happening; the plane's interior is a constant. For passengers, the worst effect of this may be some motion sickness, but pilots are trained to be wary of a second effect of this mismatch. In conditions of very low visibility, an acceleration of the plane may be misinterpreted as a climb (an upward tilt of the plane) (MacNeilage et al., 2007; Sánchez-Tena et al., 2018), a compelling phenomenon called the somatogravic illusion. Both acceleration and climb will press you back in your seat, so pilots are trained not to reflexively dive the plane (which could result in disaster), but instead to rely on their instruments rather than their vestibular systems to determine whether the plane is climbing or accelerating.
1. Use a diagram to explain how the general layout of the vestibular system allows it to track movement in three axes. Where are the receptors for head movement located? Do they resemble other types of sensory receptors? 2. Where are the vestibular nuclei located? What nerve provides inputs to these nuclei? 3. How is vestibular information used in ongoing behavior? 4. Discuss the role of the vestibular system in motion sickness.
6.5Taste: Chemicals in Foods Are Perceived as Tastes We now turn our attention to the specialized sensors that gives us our sense of taste. After reading this section, you should be able to: 6.5.1 Describe the structure, function, and distribution of the papillae on the tongue. 6.5.2 Summarize the structure of taste buds, and discuss their relationship to papillae. 6.5.3 Describe the basic tastes and the distribution of taste sensitivity across the surface of the tongue.
6.5.4 Describe the specialized cellular mechanisms through which taste cells transduce each of the major tastes. 6.5.5 Trace the neural projection of gustatory information to the brainstem and higher-order systems. Delicious foods, poisons, dangerous adversaries, and fertile mates--these are just a few of the sources of chemical signals in the environment. Being able to detect these signals is vital for survival and reproduction throughout the animal kingdom. Most people derive great pleasure from eating delicious food, and because we recognize many substances by their distinct flavors, we tend to think that we can discriminate many tastes. In reality, though, humans detect only a small number of basic tastes; the huge variety of sensations aroused by different foods are actually flavors rather than simple tastes, and they rely on the sense of smell as well as taste. (To appreciate the importance of smell to flavor, block your nose while eating first a little bit of raw potato and then some apple: without the sense of smell, you can't tell them apart!) Scientists are in broad agreement that we possess at least five basic tastes: salty, sour, sweet, bitter, and umami. (Umami, Japanese for "delicious taste," is the term for the savory, meaty taste that is characteristic of gravy or soy sauce.) These tastes are determined genetically, as we will see shortly, but there is considerable genetic variation across the globe in both the strength and pleasurable qualities of the basic tastes (Pirastu et al., 2016). Further, the hunt continues for additional basic tastes. For example, studies suggest that humans may possess a primary fat taste (Mattes, 2011); another candidate, called kokumi, is described as the full-bodied, thick, mouth-filling quality of some foods (S. C. Brennan et al., 2014). But no matter how many basic tastes we are eventually shown to possess, it is clear that evolution shaped them to help us find nutritious food and avoid toxins. Tastes excite specialized receptor cells on the tongue Many people think that the many little bumps on their tongues are taste buds, but they aren't. They are actually papillae (singular papilla) (FIGURE 6.15), tiny lumps of tissue that increase the surface area of the tongue.
flavor The sense of taste combined with the sense of smell. taste Any of the five basic sensations detected by the tongue--sweet, salty, sour, bitter, and umami. taste bud A cluster of 50-150 cells that detects tastes. Taste buds are found in papillae. papilla A small bump that projects from the surface of the tongue. Papillae contain most of the taste receptor cells.
© Science Photo Library/Alamy Stock Photo
FIGURE 6.15 A Cross Section of the Tongue
Taste bud Lining the sides of each papilla are taste buds... ...which are made up of taste receptor cells that contact tastants in saliva via ne projections called microvilli. Taste cell Microvilli
The three different types of papillae are positioned as shown.
Contrary to popular belief, receptors for all ve traditional tastes are found anywhere there are taste buds.
FIGURE 6.16 Taste Buds and Taste Receptor Cells (Part A after S. K. McLaughlin et al., 1994. Physiol. Behav. 56: 1157; C and D after L. M. Bartoshuk in D. Chadwick et al., 1993. The Molecular Basis of Smell and Taste Transduction. Wiley. New York.)
Watson/Breedlove The Mind's VMieacwhiAnectivity 6.2: Foundations of Brain and Behavior 4e Taste Buds and Taste Receptor Cells MM4e_06.16 08/31/20
There are three kinds of papillae--circumvallate, foliate, and fungiform papillae-- occurring in different locations on the tongue (FIGURE 6.16). Taste buds, each consisting of a cluster of 50-150 taste receptor cells (FIGURE 6.16B), are found buried within the walls of the papillae (a single papilla may house several such taste buds; see Figure 6.15). Fine fibers, called microvilli, extend from the taste receptor cells into a tiny pore, where they come into contact with substances that can be tasted, called tastants. Each taste cell is sensitive to just one of the five basic tastes, and with a life span of only 10-14 days, taste cells are constantly being replaced. But as our varied experience with hot drinks, frozen flagpoles, or spicy foods informs us, taste is not the only sensory capability of the tongue. It also possesses sensory cells for pain, touch, and temperature. You may have seen maps of the tongue indicating that each taste is perceived mainly in one region (sweet at the tip of the tongue, bitter at the back, and so on), but these maps are based on an enduring myth. All five basic tastes can be perceived anywhere on the tongue where there are taste receptors (Chandrashekar et al., 2006). Those areas do not differ greatly in the strength of taste sensations that they mediate (FIGURE 6.16D). The five basic tastes are signaled by specific sensors on taste cells The tastes salty and sour are evoked when taste cells are stimulated by simple ions acting on ion channels in the membranes of the taste cells. Sweet, bitter, and umami tastes are perceived by specialized receptor molecules--G protein-coupled receptors (GPCRs), as we discussed in Chapter 3 (see Figure 3.2)--that use second messengers to change the activity of the taste cell. Researchers have also discovered taste receptors in numerous tissues of the body--not just the tongue (FIGURE 6.17)--where they serve functions unrelated to conventional taste, such as the control of appetite and digestion (Behrens and Meyerhof, 2019).
SALTY Taste cells apparently sense salt (NaCl) in several different ways, which are not yet completely understood. As you might guess, one kind of salt sensor simply relies on sodium (Na+) channels, just like the ones we have seen in previous chapters. In this case, sodium ions (Na+) from salty food enter taste cells via sodium channels in the cell membrane, causing a depolarization of the cell and release of neurotransmitter. We know that this is a crucial mechanism for perceiving saltiness, because blocking the sodium channels with a drug reduces salt discrimination--though it does not eliminate it (Chandrashekar et al., 2010). This system also seems to be responsible for the appetizing qualities of moderate concentrations of salt in food. However, research indicates that taste cells are also sensitive to the other ion that is liberated when salt dissolves: chloride (Cl-). This parallel salt-sensing system seems to mediate the aversive properties of high concentrations of salt. Because drugs that block chloride-selective ion channels have little effect on the Cl- sensitivity of the tongue, researchers believe that Cl- transduction by taste cells involves a different, as-yet-unknown mechanism (Roebber et al., 2019). Depolarization of the salt-sensitive taste cells ultimately causes them to release neurotransmitters that stimulate afferent neurons that relay the information to the brain.
FIGURE 6.17 Body Tissues Expressing Taste Receptors (After an illustration by Nicole Rager Fuller in R. Ehrenberg, 2010. Science News 177: 22-25.)
Locations in which taste-related components have been found. By searching for the molecular components of the known taste receptors, researchers found taste-like sensors in a surprising variety of tissues, performing functions that are as yet unknown.
SOUR Acids in food taste sour--the more acidic the food, the more sour it tastes--but no one knows exactly how sour tastants are detected. Researchers think that the protons (H+, also called hydrogen ions) that all acids release may interact with special acid-sensing ion channels (like the ionotropic receptors in Chapter 2 and Chapter 3) to change the polarity of taste cells and alter transmitter release. It seems that all sour-sensitive taste cells contain a particular type of ion channel proteinWaantdsosnh/Bareeedalnovienward flow of protons that depolarizes the cell (A. L. Huang et al., 20T0h6e;MBiunsdh'smMaancheinteal., 2015). Foundations of Brain and Behavior 4e Interestingly, the same sensor appears to detect the sensation and taste of carbonation in drinks (Chandrashekar et al., 2009) and prompts thirstyMaMn4iem_0a6l.s17to d07ri/n20k/(2Z0occhi et al., 2017).
SWEET The receptors for sweet, bitter, and umami tastes are more like metabotropic receptors than ionotropic receptors (see Figure 3.2) because tastant molecules bind to a complex receptor protein on the taste cell's surface that activates a second messenger within the cell. These receptors are made up of simpler proteins belonging to two families--designated T1R and T2R--that are combined in various ways. When two members of the T1R family--T1R2 and T1R3--combine (heterodimerize), they make a receptor that selectively detects sweet tastants (Nelson et al., 2001). Mice engineered to lack either T1R2 or T1R3 are insensitive to sweet tastes (Zhao et al., 2003). And if you've spent any time around cats, you may be aware that they couldn't care less about sweets. It turns out that in all cats, from tabbies to tigers, the gene that encodes T1R2 is disabled, so their sweet receptors don't work (X. Li et al., 2009).
T1R A family of taste receptor proteins that, when particular members bind together, form taste receptors for sweet flavors and umami flavors. T2R A family of bitter taste receptors.
200CHAPTER6 FIGURE 6.18 It's All a Matter of Taste Buds (A)
Certain substances that taste unpleasantly bitter to most people can't be tasted at all by some people.
(B) ...than supertasters, who are extra sensitive to bitter and sweet tastants.
Courtesy of Linda Bartoshuk and the Bartoshuk Lab
umami One of the five basic tastes-- the meaty, savory flavor. (The other four tastes are salty, sour, sweet, and bitter.) gustatory system The sensory system that detects taste.
BITTER In nature, bitter tastes often signal the presence of toxins, so it's not surprising that a high sensitivity to different kinds of bitter tastes has evolved (Lush, 1989), although inWdaitvsoidn/uBarlesevdalorvyesignificantly in their taste sensitivity (FIGURE 6.18). Members of the TT2hRe Mfaimndi'lsyMoafcrheinceptor proteins appear to function as bitter receptors (Chandrashekar eFtoaunl.d, a2t0io0n0s ;ofBBerhairneannsd aBnehdavMiore4yeerhof, 2018). The T2R family has about 30 members, and tMhiMs l4aer_g0e6.1n8um0b3e/r04m/2a0y reflect the wide variety of bitter substances encountered in the environment, as well as the adaptive importance of being able to detect and avoid them. Interestingly, each bitter-sensing taste cell produces most or all of the different types of T2R bitter receptors (Adler et al., 2000). So bitter-sensing taste cells exhibit broadly tuned sensitivity to any bitter-tasting substances (Brasser et al., 2005)--just what you'd expect in a sensory system that has evolved to act as a poison detector. UMAMI The fifth basic taste, umami--the meaty, savory flavor--is detected by at least two kinds of receptors. One of these is a variant of the metabotropic glutamate receptor (Chaudhari et al., 2000; Maruyama et al., 2006) and most likely responds to the amino acid glutamate, which is found in high concentrations in meats, cheeses, kombu, and other savory foodstuffs (that's why MSG--monosodium glutamate--is used as a "flavor enhancer"). The second probable umami receptor, a heterodimer of T1R1 and T1R3 proteins, responds to most of the dietary amino acids (Nelson et al., 2002). Given this receptor's similarity to the T1R2+T1R3 sweet receptor, there is reason to suppose that receptors for things that taste good may have shared evolutionary origins. Consider the taste abilities of birds that, just like their house cat enemies, lack the T1R2 gene and thus ordinarily can't taste sweet. How then do hummingbirds sense the nectar they need for survival? It appears that evolution repurposed the hummingbird T1R1+T1R3 umami receptor into a new class of sweet receptor (Baldwin et al., 2014), allowing hummingbirds to thrive and spread. Taste information is transmitted to several parts of the brain Taste projections of the gustatory system (from the Latin gustare, "to taste") extend from the tongue to several brainstem nuclei, then to the thalamus, and ultimately to gustatory regions of the somatosensory cortex (FIGURE 6.19). Because there are only five basic tastes, and because each taste cell detects just one of the five, the encoding of taste perception could be quite straightforward, with the brain simply monitoring which specific axons are active in order to determine which tastes are present (Chandrashekar et al., 2006). In such a simple arrangement--as we noted earlier, it is sometimes called a labeled-line system--there is no need to analyze complex patterns of activity across multiple kinds of taste receptors (called pattern coding). Experimental evidence seemingly supports the conclusion that taste is a labeled-line system: selectively inactivating taste
Gustatory cortex: Anterior insula/frontal operculum Brainstem
FIGURE 6.19 Anatomy and Main Pathways of the Human Gustatory System
Thalamus Solitary tract and its nucleus Facial nerve (VII) Glossopharyngeal nerve (IX) Vagus nerve (X)
Taste information is carried in several different cranial nerves. A dedicated set of axonal projections from the thalamus projects this information to the cortical taste areas that give us our conscious experience of tastes.
cells that express receptors for just one of the five tastes tends to completely eradicate sWenastsiotinv/itByreteodtlohvaet one taste while leaving the other four tastes unaffected (Huang et al., The Mind's Machine 2F0o0u6n)d.aHtioonws oefvBerar,inthanedsBaemhaevimora4ne ipulation can also be viewed as knocking out one-fifth of any pattern of activity that would be normally present. From this perspective, the pattMerMn-4ceo_d06i.n1g9 ac0c8o/u31n/t2c0annot be ruled out. A precise understanding of the way in which the brain encodes taste information thus awaits future developments. 1. What are the five basic tastes? 2. Generate a map of the human tongue, showing how sensitive each region is to the five basic tastes. 3. Compare and contrast taste buds and papillae. 4. Identify the cellular mechanisms underlying each of the five tastes. Discuss the evolution of taste sensitivity: How do these five tastes help us survive? 6.6Smell: Chemicals in the Air Elicit Odor Sensations Finally we turn our attention to the specialized sensory system that samples chemicals in the air: our sense of smell. After reading this section, you should be able to: 6.6.1 Describe the main structures of the olfactory system, with a focus on the cells and projections of the olfactory epithelium. 6.6.2 Explain the process of olfactory transduction, and discuss the function and variety of olfactory receptors that have been discovered.
202CHAPTER6 olfaction The sensory system that detects smell; the act of smelling. odor The sensation of smell. olfactory epithelium A sheet of olfactory receptors and other cells that lines the dorsal portion of the nasal cavities and adjacent regions. View Animation 6.6: The Human Olfactory System
6.6.3 Trace the projection route of olfactory information, and main olfactory structures, from the olfactory epithelium to the cortex. 6.6.4 Compare and contrast human olfactory capabilities with those of other species. 6.6.5 Describe the structure and function of the vomeronasal system, and weigh the evidence for and against the idea that humans detect pheromones. As for all the other senses, species differences in olfaction--odor perception--reflect the evolutionary importance of various smells for survival and reproduction (Bear et al., 2016). You may have been told that humans have a poor sense of smell, but more recent evidence indicates otherwise. Although we don't know exactly how many different odors humans can discriminate between--a controversial estimate places the number as high as 1 trillion different odors (Bushdid et al., 2014), although this may be a statistical overestimation (Gerkin and Castro, 2015)--the idea that we humans have a poor sense of smell relative to other animals has been overstated historically (McGann, 2017). Our ability to perceive a large number of different odors is what produces the complex array of flavors that we normally think of as tastes. And while our olfactory system is less sensitive overall--requires stronger stimulation--than that of olfactory champions such as dogs and rabbits, most birds have only basic olfactory abilities, and dolphins don't have olfactory receptors at all. The sense of smell starts with receptor neurons in the nose In humans (and most other mammals), a sheet of cells called the olfactory epithelium lines part of the nasal cavities. Within the 5-10 square centimeters of olfactory epithelium that we possess, three types of cells are found (FIGURE 6.20): supporting cells, basal cells, and about 6 million olfactory receptor neurons. For comparison, dogs have 100-300 million olfactory receptor neurons, which explains their ability to detect odors at extremely low concentrations--as low as 2 parts per trillion (King, 2013), which is like tasting a pinch of sugar dissolved in a billion cups of tea!
Each glomerulus receives axons from olfactory receptor cells that share the same sensitivity.
Olfactory receptor cells extend ne axons into the olfactory bulbs and synapse on glomeruli.
Olfactory bulb Cribriform bone Olfactory epithelium Olfactory mucosa
Air FIGURE 6.20 The Human Olfactory System
Prepyriform cortex (primary olfactory cortex)
The rat has large olfactory bulbs relative to the size of the rest of the brain, re ecting the greater sensitivity of the rodent olfactory system, compared with that of humans (compare Figure 6.20).
FIGURE 6.21 Different Kinds of Olfactory Receptor Molecules on the Olfactory Epithelium (Part A after R. Vassar et al., 1993. Cell 74: 309.)
The color shows the distribution of members of the four receptor subfamilies; note that the olfactory bulb shows matching organization. The different receptor types have distinct but overlapping spatial distributions.
Each olfactory receptor cell is a complete neuron, with a long, slender apical dendrite that divides into branches (cilia) that extend into the moist mucosal surface. Substances that we can smell from the air that we inhale or sniff, called odorants, dissolve Watson/Breedlove TinhetoMtihnde'smMuaccohsinael layer and interact with receptors studding the dendritic cilia of the Foolufnadcattoiornys nofeBurraoinnasnd(MBeohahvriohra4redt et al., 2018). Like the metabotropic receptors found on neurons, the olfactory receptor proteins are a variety of G protein-coupled receptors MM4e_06.21 07/20/20 (GPCRs), employing a second-messenger system to respond to the presence of odorants. However, despite these similarities, olfactory neurons differ from the neurons of the brain in several ways. One way in which olfactory neurons are distinct from their cousins in the brain relates to the production of receptors: there is an incredible diversity of olfactory receptor protein subtypes. So, while there may be up to a dozen or so subtypes of receptors for a given neurotransmitter in the brain, there are hundreds or even thousands of subtypes within the family of odorant receptors, depending on the species under study. The Nobel Prize-winning discovery of the genes encoding this odorant receptor superfamily (Buck and Axel, 1991) provided one of the most important advances in the history of olfaction research. Mice have about 2 million olfactory receptor neurons, each of which expresses only one of about 1,000 different receptor proteins. These receptor proteins can be divided into four different subfamilies of about 250 receptors each (Mori et al., 1999). Within each subfamily, members have similar structure and presumably recognize chemically similar odorants. Receptors of different subfamilies are expressed in separate bands of olfactory neurons within the olfactory epithelium (FIGURE 6.21) (Coleman et al., 2019). By comparison, humans make a total of about 400 different kinds of functional olfactory receptor proteins. That's still a large number, but in our case, it looks like hundreds of additional olfactory receptor genes have become nonfunctional during the course of evolution (Olender et al., 2008), suggesting that the substances they detected ceased to be important to our ancestors' survival and reproduction. And in a curious parallel to the discovery of taste receptors throughout the body, it turns out that some of the tongue's taste cells possess functional olfactory receptors (Malik et al., 2019), perhaps reflecting the great importance of flavors to our species. Whatever turns out to be the actual number of odors humans can distinguish, our ability to discriminate thousands, millions, or perhaps billions of odors using just 400 kinds
204CHAPTER6 olfactory bulb An anterior projection of the brain that terminates in the upper nasal passages and, through small openings in the skull, provides receptors for smell. glomerulus A complex arbor of dendrites from a group of olfactory cells.
Orbitofrontal cortex (secondary olfactory cortex)
Prepyriform cortex (primary olfactory cortex)
Olfactory bulb Olfactory receptors FIGURE 6.22 Components of the Brain's Olfactory System
of functional olfactory receptors indicates that we must recognize most odorants by their activation of a characteristic combination of different kinds of receptor molecules (Duchamp-Viret et al., 1999), an example of pattern coding. In addition, any two people will differ by about 30% in the makeup of their olfactory receptors (Mainland et al., 2014), so to some extent we each live in our own, personalized olfactory world (Trimmer et al., 2019). Another big difference between olfactory neurons and brain neurons is that olfactory neurons die and are replaced in adulthood (Lledo and Valley, 2018). This regenerative capacity is most likely an adaptation to the hazardous environment that olfactory neurons inhabit. If an olfactory neuron is killed--say, by the virus that gave you that darn head cold, or by a whiff of something toxic while you were cleaning out the shed, or by some other misadventure--an adjacent basal cell will soon differentiate into a neuron and begin extending a dendrite and an axon (Leung et al., 2007). Each olfactory neuron extends a fine, unmyelinated axon into the nearby olfactory bulb of the brain, where it terminates on one specific glomerulus--a spherical clump of neurons (from the Latin glomus, "ball")--out of the thousands that exist in the olfactory bulb. Each glomerulus receives inputs exclusively from olfactory neurons that are expressing the same type of olfactory receptor (see Figure 6.20). No one knows exactly how the extending axon knows where to go to find its specific glomerulus, or how it knows where to form synapses within the glomerulus after it arrives. One possibility is that olfactory receptor proteins that are found on the axons of these cells (as well as on the dendrites) guide the axons to their corresponding glomeruli (Barnea et al., 2004; Imai et al., 2009). But whatever may be the exact mechanisms of neuroplasticity in these cells, better understanding of the process of olfactory neurogenesis may someday help us develop methods for restoring damaged regions of the brain and spinal cord. Olfactory information projects from the olfactory bulbs to several brain regions Having received information from multiple olfactory neurons all expressing the same type of olfactory receptor, the glomerulus then actively tunes and sharpens the neural activity associated with the corresponding odorants (Aungst et al., 2003). The glomeruli are organized within the olfactory bulb according to an orderly, topographic map of smells, with neighboring glomeruli receiving inputs from receptors that are closely related. And, as Figure 6.21 shows, the spatial organization of glomeruli within the olfactory bulbs reflects the segregation of the four receptor protein subfamilies in the olfactory epithelium (Mori et al., 1999). This glomerular organization is established during a critical period in early life, after which it becomes fixed (Tsai and Barnea, 2014), resulting in an "olfactotopic" map that is maintained within the olfactory projections throughout the brain. Olfactory information is conveyed to the brain via the axons of mitral cells (see Figure 6.20), which extend from the glomeruli in the olfactory bulbs to various regions of the forebrain; smell is the only sensory modality that synapses directly in the cortex rather than having to pass through the thalamus. Important targets for olfactory inputs include the hypothalamus, the amygdala, and the prepyriform cortex (FIGURE 6.22). These limbic structures are closely involved in memory and emotion, which may help explain the potency of odors in evoking nostalgic memories of childhood (M. Larsson and Willander, 2009). Many vertebrates possess a vomeronasal system Though many perfumers have tried to create one, there is no perfume for humans that is as alluring as the natural scents that other species use to find possible mates. The majority of terrestrial vertebrates--mammals, amphibians, and reptiles--possess a secondary chemical detection system that is specialized for detecting such
Vomeronasal nerves Vomeronasal organ (VNO)
FIGURE 6.23 The Vomeronasal System (After R. Vassar et al. 1993. Cell 74: 309.)
Wphatesroonm/Boreneedslo.vTehe system is called the vomeronasal system (FIGURE 6.23), and its reTcheeptMoirnsda'sreMfaocuhinnde in the vomeronasal organ (VNO), near the olfactory epithelium. Foundations of Brain and Behavior 4e In rodents, the sensory neurons of the VNO make hundreds of different vomMerMon4ea_s0a6l.2r3ece0p6t/o0r4/p2r0oteins, forming two large families of GPCRs called V1R and V2R (Dulac and Torello, 2003). These receptors are extremely sensitive, able to detect very low levels of the pheromone signals--such as sex hormone metabolites and signals of genetic relatedness--that are released by other individuals (Leinders-Zufall et al., 2000; Loconto et al., 2003). From the VNO, information is transmitted to the accessory olfactory bulb (adjacent to the main olfactory bulb), which projects to the medial amygdala and hypothalamus, structures that play crucial roles in governing emotional and sexual behaviors and in regulating hormone secretion. Hamsters and mice can distinguish relatives from nonrelatives just by smell (Mateo and Johnston, 2000; Isles et al., 2001), allowing these animals to optimize their reproductive activities. In parallel, dedicated mechanisms in olfactory cortex activate fear and stress responses to predator odor signals, helping the animal to avoid their toothy source (Kondoh et al., 2016). Do humans communicate via pheromones? Studies reporting pheromone-like phenomena in humans attract plenty of media attention because of the apparent link to our evolutionary past. Well-known examples include the report that simple exposure to each other's bodily odors can shift women's menstrual cycles (Stern and McClintock, 1998) and a report that exposure to female tears causes reductions in testosterone and sexual arousal in men (Gelstein et al., 2011). However, the VNO is either vestigial or absent in humans, and almost all of our V1R and V2R receptor genes have become nonfunctional "pseudogenes" over evolutionary time (Lübke and Pause, 2015). So, if humans do communicate through pheromones, it is most likely accomplished using the main olfactory epithelium, and not the VNO. In mice, receptors in
pheromone A chemical signal that is released outside the body of an animal and affects other members of the same species. vomeronasal organ (VNO) A collection of specialized receptor cells, near to but separate from the olfactory epithelium, that detect pheromones and send electrical signals to the accessory olfactory bulb in the brain.
trace amine-associated receptor (TAAR) Any one of a family of probable pheromone receptors produced by neurons in the main olfactory epithelium.
the main olfactory epithelium called TAARs, for trace amine-associated receptors, reportedly respond to sex-specific pheromones instead of odorants (Liberles and Buck, 2006), and mice with their TAAR genes knocked out stop reacting to certain urinary odor signals, even in the urine of predators (Dewan et al., 2013). Thus, the old notion that the olfactory epithelium detects odors while the VNO detects pheromones is an oversimplification, even in rodents. And because TAARs have also been found in the human olfactory epithelium (Liberles, 2009), behavioral evidence indicating that humans respond to pheromones no longer presents a paradox. If rodents can detect pheromones through the olfactory epithelium, using TAARs or other yet-unknown mechanisms, then perhaps we can too. Whatever the details of the mechanism may be, evidence is rapidly accumulating that odor is an ecologically important channel for human social communication (J. H. de Groot et al., 2017).
1. Discuss odor sensitivity in humans. How do we compare with other species? 2. Provide a brief sketch of the olfactory epithelium, showing the major cell types and their relationships to the brain. 3. Discuss the genetics of odor receptors, as well as their spatial organization in the nose and olfactory bulbs. What is a glomerulus? 4. Which regions of the brain receive strong olfactory inputs? What is the significance of this arrangement for an animal's behavior? 5. Discuss the structures and receptors associated with pheromone sensitivity, and speculate about the ecological importance of pheromone sensitivity in humans and other animals. Are humans sensitive to pheromones? Recommended Reading Doty, R. L. (2015). Handbook of Olfaction and Gustation (3rd ed.). New York, NY: Wiley-Blackwell. Hawkes, C. H. (2018). Smell and Taste Disorders. Cambridge, UK: Cambridge University Press. Horowitz, S. S. (2012). The Universal Sense: How Hearing Shapes the Mind. London, UK: Bloomsbury. Musiek, F. E., and Baran, J. A. (2018). The Auditory System: Anatomy, Physiology, and Clinical Correlates (2nd ed.). San Diego, CA: Plural. Palmer, A., and Rees, A. (2010). Oxford Handbook of Auditory Science. Oxford, UK: Oxford University Press. Wolfe, J. M., Kluender, K. R., Levi, D. M., Bartoshuk, L. M., et al. (2021). Sensation & Perception (6th ed.). Sunderland, MA: Oxford University Press/Sinauer. Wyatt, T. D. (2014). Pheromones and Animal Behavior: Chemical Signals and Signatures (2nd ed.). Cambridge, UK: Cambridge University Press. Yost, W. A. (2013). Fundamentals of Hearing (5th ed.). San Diego, CA: Academic Press.
6 · VISUAL SUMMARY You should be able to relate each summary to the adjacent illustration, including structures and processes. The online version of this Visual Summary includes links to figures, animations, and activities that will help you consolidate the material.
1 The pinna (external ear) captures, focuses, and filters sound. The sound arriving at the tympanic membrane (eardrum) is focused by the three ossicles of the middle ear onto the oval window to stimulate the fluid-filled inner ear (specifically, the cochlea). Review Figure 6.1, Animations 6.2 and 6.3 3 Movement of the stereocilia of the hair cells causes the opening and closing of ion channels, thereby transducing mechanical movement into changes in electrical potential. The hair cell then releases neurotransmitter to simulate the nerve cell endings that contact them. Review Figure 6.3 5 Afferents from the inner hair cells transmit auditory information to the cochlear nuclei of the brainstem. Cochlear neurons project bilaterally to the superior olivary nucleus, which in turn innervates the inferior colliculus. From there auditory information is relayed to the medial geniculate nucleus and then the primary auditory cortex in the temporal lobe. Review Figure 6.5, Animation 6.4
2 Sound arriving at the oval window causes traveling waves to sweep along the basilar membrane of the cochlea. For sounds of high frequency, the largest displacement of the basilar membrane is at the base of the cochlea, near the oval window; for low-frequency sounds, the largest amplitude is near the apex of the cochlea. Review Figure 6.2, Box 6.1 4 The organ of Corti has both inner hair cells (IHCs, about 3,500 in humans) and outer hair cells (OHCs, about 12,000 in humans). The inner hair cells convey most of the information about sounds. The outer hair cells change their length under the control of the brain, amplifying the movements of the basilar membrane in response to sound and sharpening the frequency tuning of the cochlea. Review Figure 6.3, Activity 6.1 6 Auditory localization depends on differences in the sounds arriving at the two ears. For low-frequency sounds, interaural temporal differences (differences in time of arrival at the two ears) are especially important. For high-frequency sounds, interaural intensity differences are especially important, and spectral filtering provides cues about elevation. Review Figure 6.7
7 Primary auditory cortex is specialized for processing complex, biologically important sounds, rather than pure tones. Experiences with sound early in life can influence later auditory localization and the responses of neurons in auditory pathways. Experiences later in life can also lead to changes in the responses of auditory neurons. Review Figures 6.8 and 6.9 9 Some forms of deafness may be alleviated by direct electrical stimulation of the auditory nerve by a cochlear implant. Genetic manipulations can induce new hair cell growth in laboratory animals, raising hope of a gene therapy for sensorineural deafness. Review Figure 6.13
8 Conduction deafness consists of impairments
in the transmission of sound through the exter-
nal or middle ear to the cochlea. Sensorineural
deafness arises in the cochlea, often because
of the destruction of hair cells, or in the audi-
tory nerve. Central deafness stems from brain
10 The receptors of the vestibular system that detect movement of the head lie within the inner ear next to the cochlea. In mammals the vestibular system consists of three semicircular canals plus the utricle and the saccule. The semicircular canals use hair cells to detect rotation of the body in three planes, and the utricle and saccule sense static positions and linear accelerations. Review Figure 6.14, Animation 6.5
11 Humans detect only five main tastes--salty, sour, sweet, bitter, and umami--using taste receptor cells located in clusters called taste buds. Taste cells extend fine filaments into the taste pore of each bud, where tastants come into contact with them. The taste buds are situated on small projections from the surface of the tongue called papillae. The tastes of salty and sour are evoked primarily by the movement of ions (usually from food) through ion channels in the membranes of taste cells. Sweet, umami, and bitter tastes are perceived by specialized G protein-coupled receptors (GPCRs) belonging to the T1R and T2R families. Taste receptors are also expressed in tissues elsewhere in the body. Review Figures 6.16 and 6.17, Activity 6.2
12 Each taste cell transmits information via cranial nerves to brainstem nuclei. This gustatory system extends from the taste receptor cells through brainstem nuclei to the thalamus and then to the cerebral cortex. Each taste axon responds most strongly to one category of tastes, providing a labeled line to the brain. Review Figure 6.19 14 There is a large family of odor receptor molecules, each of which utilizes G proteins and second messengers. Large subfamilies of receptors are synthesized in distinct bands of the olfactory epithelium. Review Figure 6.21 16 The vomeronasal organ (VNO) contains receptors to detect pheromones released from other individuals of the species. These receptors transmit signals to the accessory olfactory bulb, which in turn communicates with the amygdala. Pheromones can also be detected by specialized receptors in the main olfactory epithelium. Review Figure 6.23
13 In contrast to being able to detect only a few tastes, humans can detect a huge number of different odors. Olfactory receptor neurons extend dendrites in the olfactory epithelium that express olfactory receptor proteins. The fine, unmyelinated axons of olfactory neurons project to the olfactory bulbs and synapse within glomeruli. If an olfactory receptor cell dies, an adjacent cell will replace it. Review Figure 6.20, Animation 6.6
Orbitofrontal cortex (secondary olfactory cortex)
Prepyriform cortex (primary olfactory cortex)
15 Outputs from the olfactory bulb extend to prepyriform cortex, amygdala, and hypothalamus, among other brain regions. Olfactory projections to the cortex maintain a stereotyped olfactory map of slightly overlapping projections from the glomeruli. Review Figure 6.22
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