hearing

hearing Sounds are rapid variations in pressure, which are propagated through the air away from a vibrating object, such as a loudspeaker cone or the human vocal cords. Our sense of hearing allows us to detect and identify the myriad sounds present in our environment, and to determine their whereabouts. In humans and other animals with a poorly-developed sense of smell, hearing plays a particularly important role in alerting the listener to novel events in the environment. Through speech and music, human hearing also makes an extremely important contribution to social communication.

When the prongs of a tuning fork vibrate back and forth in a regular manner, a periodic sound is produced. For such a pure tone, the simplest type of sound, the pressure increases and then decreases following a smooth wave pattern (a sinusoidal function). The number of complete cycles per second is known as the frequency of the tone and is measured in Hertz (Hz). More commonly, natural sounds contain a number of different frequency components, the variation in intensity across the frequency range being referred to as the spectrum of the sound. The fundamental frequency of a complex tone corresponds to its perceived pitch, whereas the full spectrum determines the timbre, or sound quality. Thus, the same note played on two different musical instruments may sound different, as a result of differences in the additional frequencies in their spectra.

Young, healthy humans can hear sound frequencies from about 40 Hz to 20 kHz, although the upper frequency limit declines with age. Other mammals can hear frequencies that are inaudible to humans, both lower and higher. Some bats, for example, which navigate by echolocation, both emit and hear sounds with frequencies of more than 100 kHz. In general, there is a good match between the sound frequencies to which an animal is most sensitive and those frequencies it uses for communication. This is true in humans, who are most sensitive over a broad range of tones that cover the spectrum of human speech.

Compared with total atmospheric pressure, airborne sound waves represent extremely small pressure changes. The amplitude of the pressure variation in a sound directly determines its perceived loudness. Because the range of sound pressures that can be heard is so large, a logarithmic scale of decibels (dB) is used to measure sound intensity. On this scale, 0 dB is around the lowest sound level that can be heard by a human listener, whereas sound levels of 100 dB or more are uncomfortably loud and may damage the ears. At pop concerts and in discos the sound level can be much higher than this!

The design of the ear changed substantially between aquatic and terrestrial vertebrates, but has remained very similar among mammals (except for specializations for different parts of the frequency spectrum). The human ear is illustrated in the figure. It is subdivided into the external, middle, and inner ear. The visible part of the ear comprises the skin-covered cartilaginous external ear. This includes the pinna on the side of the head and the external auditory meatus, or ear canal, which terminates at the eardrum. As they travel into the ear canal, sounds are filtered so that the amplitude of different frequency components is altered in different ways depending on the location of the sound source. These spectral modifications, which are not perceived as a change in sound quality, help us to localize the source of the sound. They are particularly important for distinguishing between sounds located in front of and behind or above and below the listener, and for localizing sounds if you are deaf in one ear, or when listening to very quiet sounds, inaudible to one ear. Because of its resonance characteristics, the external ear also amplifies the sound pressure at the eardrum by up to 20 dB in humans over a frequency range of 2–7 kHz.

Lying behind the eardrum is an air-filled cavity known as the middle ear, which is connected to the back of the throat via the eustachian tube. Opening of this tube during swallowing and yawning serves to maintain the middle ear cavity at atmospheric pressure. Airborne sounds pass through the middle ear to reach the fluid-filled cochlea of the inner ear, where the process of transduction — the conversion of sound into the electrical signals of nerve cells — takes place. Because of its greater density, the fluid in the cochlea has a much higher resistance to sound vibration than the air in the middle ear cavity. To avoid most of the incoming sound energy from being reflected back, vibrations of the eardrum are mechanically coupled to a flexible membrane (the oval window) in the wall of the cochlea by the three smallest bones in the body (the malleus, incus, and stapes — together known as the ossicles). These delicately suspended bones improve the efficiency with which sound energy is transferred from the air to the fluid in the cochlea and therefore prevent the loss in sound pressure that would otherwise occur due to the higher impedance of the cochlear fluids. This is achieved primarily because the vibrations of the eardrum are concentrated on the much smaller footplate of the stapes, which fits into the oval window of the cochlea. The smallest skeletal muscles in the body are attached to the ossicles, and contract reflexly in response to loud sounds or when the owner of them speaks. These contractions dampen the vibrations of the ossicles, thereby reducing the transmission of sound through the middle ear. As with the external ear, the efficiency of middle ear transmission varies with sound frequency. Together, these structures determine the frequencies to which we are most sensitive.

The inner ear includes the cochlea, the hearing organ, and the semicircular canals and otolith organs, the sense organs of balance. Both systems employ specialized receptor cells, known as hair cells, for detecting mechanical changes within the fluid-filled inner ear. Projecting from the apical surface of each hair cell is a bundle of around 100 hairs called stereocilia. Deflection of the bundle of hairs by sound (in the cochlea) or head motion or gravity (in the balance organs) leads to the opening of pores in the membrane of the hairs that allow small, positively-charged ions to rush into the hair cell and change its internal voltage. This causes a neurotransmitter to be released from the base of the hair cell, which, in turn, activates the ends of nerve fibres that convey information from the ear towards the brain. Although there are some differences between the hair cells of the hearing and balance organs, they work in essentially the same way.

The mammalian cochlea is a tube which is coiled so that it fits compactly within the temporal bone. The length of the cochlea — just over 3 cm in humans — is related to the range of audible frequencies rather than the size of the animal. Consequently, this structure does not vary much in size between mice and elephants. It is subdivided lengthwise into two principal regions by a collagen-fibre meshwork known as the basilar membrane. Around 15 000 hair cells, together with the nerves that supply them and supporting cells, are distributed in rows along its length. Vibrations transmitted by the middle ear ossicles to the oval window produce pressure gradients between the cochlear fluids on either side of the basilar membrane, setting the membrane into motion. The hair cells are ideally positioned to detect very small movements of the basilar membrane. There are two types of hair cells in the cochlea. The inner hair cells form a single row, whereas the more numerous outer hair cells are typically arranged into three rows.

In the nineteenth century, the great German physiologist and physicist Hermann von Helmholtz proposed that our perception of pitch arises because each region of the cochlea resonates at a different frequency (rather like the different strings of a piano). The first direct measurements of the response of the cochlea to sound were made by Georg von Békésy a century later, on the ears of human cadavers. He showed that very loud sounds induced a travelling wave of displacement along the basilar membrane, which resembles the motion produced when a rope is whipped. Von Békésy observed that the wave built up in amplitude as it travelled along the membrane and then decreased abruptly. For high-frequency sounds, the peak amplitude of the wave occurs near the base of the cochlea (adjacent to the middle ear), whereas the position of the peak shifts towards the other end of the tube (the apex) for progressively lower frequencies. This indeed occurs because the basilar membrane increases in width and decreases in stiffness from base to apex. These observations, which led to von Békésy winning the Nobel Prize, established that the cochlea performs a crude form of Fourier analysis, splitting complex sounds into their different frequency components along the length of the basilar membrane.

More recently, much more sensitive techniques, which can measure vibrations of less than a billionth of a metre, have revealed that motion of the basilar membrane is dramatically different in living and dead preparations. In animals in which the cochlea is physiologically intact, the movements of the basilar membrane are amplified, giving rise to much greater sensitivity and sharper frequency ‘tuning’ than can be explained by the variation in width and stiffness along its length. This amplifying step most likely involves the living outer hair cells, which, when stimulated by sound, actively change their length, shortening and lengthening up to thousands of times per second. These tiny movements appear to feed energy back into the cochlea to alter the mechanical response of the basilar membrane. Damage to the outer hair cells, following exposure to loud sounds or ‘ototoxic’ drugs, leads to poorer frequency selectivity and raised thresholds of hearing. The active responses of the outer hair cells are probably responsible for the extraordinary fact that the ear itself produces sound, which can be recorded with a microphone placed close to the ear and used to provide an objective measure of the performance of the ear.

Vibrations of the basilar membrane, detected by the inner hair cells, are transmitted to the brain in the form of trains of nerve impulses passing along the 30 000 axons of the auditory nerve (which mostly make contact with the inner hair cells). Each nerve fibre responds to motion of a limited portion of the basilar membrane and is therefore tuned to a particular sound frequency. Consequently, the frequency content of a sound is represented within the nerve and the auditory regions of the brain by which fibres are active. For frequencies below about 5 kHz, the auditory nerve fibres act like microphones, in that the impulses tend to be synchronized to a particular phase of the cycle of the stimulus. This property, known as phase-locking, allows changes in sound frequency to be represented to the brain by differences in the timing of action potentials and is thought to be particularly important for pitch perception at low frequencies and for speech perception. The intensity of sound is represented within the auditory system by the rate of firing of individual neurons — the number of nerve impulses generated per second — and by the number of neurons that are active.

Auditory signals are relayed through various nuclei (collections of nerve cell bodies) in the brain stem and thalamus, up to the temporal lobe of the cerebral cortex. At each nucleus, the incoming fibres that relay information to the next group of nerve cells are distributed in a topographic order, preserving the spatial relationships of the regions of basilar membrane from which they receive information. This spatial ordering of nerve fibres establishes a neural ‘map’ of sound frequency in each nucleus. The extraction of biologically important information — ‘What is the sound? Where did it come from?’ — takes place in the brain. As a result of the complex pattern of connections that exist within the auditory pathways, many neurons, particularly in the cortex, respond better to complex sounds than to pure tones. Indeed, in certain animals, including songbirds and echolocating bats, physiologists have discovered neurons that are tuned to behaviourally important acoustical features (components of bird song or bat calls). But auditory processing reaches its zenith in humans, where different regions of the cerebral cortex appear (according to studies involving imaging techniques) to have specialized roles in the perception of language and music.

The ability to localize sounds in space assumes great importance for animals seeking prey or trying to avoid potential predators, and also when directing attention towards interesting events. Although sounds can be localized using one ear alone, an improvement in performance is usually seen if both ears hear the sound. Such binaural localization depends on the detection of tiny differences in the intensity or timing of sounds reaching the two ears. At the beginning of the twentieth century, Lord Rayleigh demonstrated that human listeners can localize sounds below about 1500 Hz using the minute differences between the time of arrival (or phase) of the sound at the two ears, which arise because the sound arrives slightly later at the ear further from the sound source. He also showed that interaural intensity differences, which result from the acoustical ‘shadow’ cast by the head, are effective cues at higher frequencies. Using these cues, listeners can distinguish two sources separated by as little as 1° in angle in the horizontal plane.

Studies in animals have shown that neurons in auditory nuclei of the brain stem receive converging signals from the two ears. By comparing the timing of the phase-locked nerve impulses coming from each side, some of these neurons show sensitivity to differences in the sound arrival time at the two ears of the order of tens of microseconds, whereas other neurons are exquisitely sensitive to interaural differences in sound level. As well as facilitating the localization of sound sources, binaural hearing improves our ability to pick out particular sound sources, which helps us to detect and analyze them, particularly against a noisy background (aptly termed the ‘cocktail party effect’).

Andrew J. King

Bibliography

Moore, B. C. J. (1997). An introduction to the psychology of hearing, (4th edn). Academic Press, London.
Pickles, J. O. (1988). An introduction to the physiology of hearing, (2nd edn). Academic Press, London.

See also deafness; ear, external; eustachian tube; hearing aid; sense organs; sensory integration; tinnitus.