Auditory information ascends to the cerebral cortex through the thalamus. Neurons of the inferior colliculus project to the medial geniculate body, where principal cells in turn project to the auditory cortex. The pathways from the inferior colliculus include a lemniscal or core pathway and extralemniscal or belt pathways. Descending projections from the auditory cortex to the medial geniculate body are prominent both anatomically and functionally.
The Auditory Cortex Maps Numerous Aspects of Sound
Ascending auditory pathways terminate in the auditory cortex, which includes multiple distinct areas on the dorsal surface of the temporal lobe. The most prominent projection is from the ventral division of the medial geniculate nucleus to the primary auditory cortex (A1, or Brodmann area 41). As in the lower relays of auditory processing, this cytoarchitectonically distinct region contains a tonotopic representation of characteristic frequencies: Neurons are arrayed in a systematic map reflecting the frequencies that best stimulate them. Neurons tuned to low frequencies are found at the rostral end of A1, and those responsive to high frequencies in the caudal region (Figure 31–11). Thus, like the visual and somatosensory cortices, the primary auditory cortex contains a map reflecting the pattern of peripheral sensors.
The auditory cortex of primates has multiple primary and secondary areas.
The expanded figure shows the major tonotopic map of the primary auditory cortex. The primary areas are surrounded by higher-order areas (see Figure 31–13).
Because the cochlea encodes only frequency, however, a one-dimensional map from the periphery is spread across the two-dimensional surface of the cortex, with a smooth frequency gradient in one direction and iso-frequency contours along the other direction. In many animals subregions of the auditory cortex representing biologically significant frequencies are enlarged because of extensive inputs, similar to the large area in the primary visual cortex devoted to inputs from the fovea.
In addition to frequency, other features of auditory stimuli are mapped in the primary auditory cortex, although the overall organization is less clear and precise than for vision. Auditory neurons in A1 are excited by input from both ears (EE), with the contralateral input usually stronger than the ipsilateral contribution, or by unilateral input (EI). The EI neurons are inhibited by stimulation of the opposite ear. Summation columns of EE neurons alternate with suppression columns of EI neurons, especially in the high-frequency portion of A1, creating a map of interaural interactions at right angles to the axis of tonotopic mapping. This partitions the auditory cortex into columns responsive to every audible frequency and each type of binaural interaction.
Certain neurons in A1 also seem to be organized according to bandwidth, that is, according to their responsiveness to a narrow or broad range of frequencies. Distinct subregions of A1 form clusters of cells with narrow or broadband tuning within individual iso-frequency contours. Synaptic connections within the cortex respect these clusters, with neurons receiving intracortical input primarily from neurons with similar bandwidths and characteristic frequencies. This modular organization of bandwidth selectivity may allow redundant processing of incoming signals through neuronal filters of varying bandwidths as well as center frequencies, which could be useful for the analysis of spectrally complex sounds such as species-specific vocalizations, including speech.
Several other parameters are mapped on the surface of A1. These include neuronal response latency, loudness, modulation of loudness, and the rate and direction of frequency modulation. Although it remains to be seen how these various maps intersect, this array of parameters clearly endows each neuron and each location in A1 with the ability to represent many independent variables of sound and generates a great diversity of neuronal selectivity.
As is true for visual and somatosensory areas of the cortex, sensory representation in A1 can change in response to altered input. After peripheral hearing loss, tonotopic mapping can be altered so that neurons originally responsive to sounds within the range of the hearing loss begin to respond to adjacent frequencies. The work of Michael Merzenich and others has shown that behavioral training of adult animals can also result in large-scale reorganization of auditory cortex, so that the most behaviorally relevant frequencies—those specifically associated with attention or reinforcement—come to be overrepresented.
The auditory areas of young animals are particularly plastic. In rodents the frequency organization of A1 emerges gradually during development from an early, crude frequency map. Raising animals in acoustic environments in which they are exposed to repeated tone pulses of a particular frequency results in a persistent expansion of cortical areas devoted to that frequency, accompanied by a general deterioration and broadening of the tonotopic map. This result not only suggests that the development of A1 is experience-dependent, but raises the possibility that early exposure to abnormal sound environments can create long-term disruptions of high-level sensory processing. A greater understanding of how this happens and whether it is also true for human fetuses and infants may provide insights into the origin and remediation of disorders in which auditory processing is centrally impaired, such as many forms of dyslexia. Moreover, the ability to induce synaptic changes in adult auditory cortex by engaging attention or reward raises new hopes for brain repair even in adulthood.
Auditory Information Is Processed in Multiple Cortical Areas
The primary auditory area of mammals is surrounded by multiple distinct regions, many of which are tonotopic. These highly tonotopic areas resemble A1 in that they receive direct input from the ventral division of the medial geniculate nucleus. Like the major thalamocortical visual projection, this input primarily contacts cortical layers IIIb and IV. Adjacent tonotopic fields have mirror-image tonotopy: The direction of tono-topy reverses at the boundary between fields.
As many as 7 to 10 secondary (belt) areas surround 3 to 4 primary or primary-like (core) areas (see Figure 31–13). These cortical areas receive input from the core areas of auditory cortex and in some cases from thalamic nuclei. Electrophysiological and imaging studies have confirmed that the primary auditory cortex in humans lies on Heschl's gyrus, in the temporal lobe, medial to the sylvian fissure. In addition, recent functional magnetic-resonance imaging studies have revealed that in humans, just as in monkeys, pure tones activate primarily core regions, whereas the neurons of belt areas prefer complex sounds such as narrow-band noise bursts.
Insectivorous Bats Have Cortical Areas Specialized for Behaviorally Relevant Features of Sound
Although it is generally assumed that the upstream auditory areas perform increasingly specialized functions related to hearing, our knowledge about the functions of serial relays is much less in the auditory system than the visual system. In humans one of the most important aspects of audition is its role in processing language, but we know relatively little about how speech sounds are analyzed by neural circuits. New techniques for imaging the human brain are gradually providing insights into the localization of cortical areas associated with language (see Chapter 60).
The best evidence for specialized analysis of complex auditory signals in auditory cortical areas comes from studies of insectivorous bats. These animals find their prey almost entirely through echolocation, emitting ultrasonic pulses of sound that are reflected by flying insects. Bats analyze the timing and structure of the echoes to help locate and identify the targets, and discrete auditory areas are devoted to processing different aspects of the echoes.
Many bats, such as the mustached bat studied by Nobuo Suga and his collaborators, emit echolocating pulses with two components. An initial constant-frequency (CF) component consists of several harmonically related sounds or harmonics. These harmonics are emitted stably for tens to hundred of milliseconds, akin to human vowel sounds. The constant-frequency component is followed by a sound that steeply decreases in frequency, the frequency-modulated (FM) component, which resembles the rapidly changing frequencies of human consonants (Figure 31–12A).
The auditory system of the bat has specialized areas for locating sounds.
A. A sonogram of an animal's calls (solid lines) and the resultant echoes (dashed lines) illustrates the two components of the call: the protracted, harmonically related constant-frequency (CF) signal and the briefer frequency-modulated (FM) signal. The duration of the calls decreases as the animal approaches its target.
B. A view of the cerebral hemisphere of the mustached bat shows three of the functional areas within the auditory cortex. The FM area is where the distance from the target is computed; the CF area is where the velocity of the target is computed; and the Doppler-shifted CF area is specialized for the identification of small fluttering objects. The expanded cortical representation of Doppler-shifted CFs near the second harmonic of the call frequency (60 to 62 kHz) forms the acoustic "fovea."
C. An FM-FM combination-sensitive neuron does not respond significantly to either pulses or echoes alone, but responds very strongly to a closely paired pulse and echo. However, the neuron is also sensitive to the time difference between the pulse and echo, as seen in the record on the right, where the neuron fails to respond to a pulse-echo combination that is not closely paired. (Modified, with permission, from Suga et al. 1983).
The FM sounds are used to determine the distance to the target. The bat measures the interval between the emitted sound and the returning echo, which corresponds to a particular distance, based on the relatively constant speed of sound. Neurons in the FM-FM area of auditory cortex (Figure 31–12B) respond preferentially to pulse-echo pairs separated by a specific delay. Moreover, these neurons respond better to particular combinations of sounds than to the individual sounds in isolation; such neurons are called feature detectors (Figure 31–12C). The FM-FM area contains an array of such detectors, with preferred delays systematically ranging from 0.4 ms to 18 ms, corresponding to target ranges of 7 cm to 310 cm, mapped along the cortical surface (see Figure 31–12B). These neurons are organized in columns, each of which is responsive to a particular combination of stimulus frequency and delay. In this way the bat, like the barn owl in its inferior colliculus, is able to represent an acoustic feature that is not directly represented by sensory receptors.
The CF components of bat calls are used to determine the relative speed of the target with respect to the bat and the acoustic image of the target. When an echolocating bat is flying toward an insect, the sounds reflected from the insect are Doppler-shifted to a higher frequency at the bat's ear, for the bat is moving toward the returning sound waves from the target, causing a relative speeding up of these waves at its ear. Similarly, a receding insect yields reflections of lowered frequency at the bat's ear. Neurons in the CF-CF area (see Figure 31–12B) are sharply tuned to a combination of frequencies close to the emitted frequency or its harmonics. Each neuron responds best to a combination of a pulse of a particular fundamental frequency and an echo corresponding to the first or second harmonic of the pulse, Doppler-shifted to a specific extent. As in the FM-FM area, neurons do not respond to the pulse or echo alone, but rather to the combination of the two CF signals.
CF-CF neurons are arranged in columns, each encoding a particular combination of frequencies. These columns are arranged regularly along the cortical surface, with the fundamental frequency along one axis and the echo harmonics along a perpendicular axis. This dual-frequency coordinate system creates a map wherein a specific location corresponds to a particular Doppler shift and thus a particular target velocity, ranging systematically from –2 m/s to 9 m/s.
The CF components of returning echoes are also used for detailed frequency analysis of the acoustic image, presumably important in its identification. The Doppler-shifted constant-frequency area (DSCF) of the mustached bat is a dramatic expansion of the primary auditory cortex's representation of frequencies between 60 kHz and 62 kHz, corresponding well to the set of returning echoes from the major CF component of the bat's call (see Figure 31–12B). Within the DSCF area individual neurons are extremely sharply tuned to frequency, so that the tiny changes in frequency created by fluttering moth wings are easily detected.
Transient inactivation of some of these specialized cortical areas, while the bat performs a discrimination task, strikingly supports the importance of their functional specialization in behavior. Silencing of the DSCF selectively impairs fine frequency discrimination while leaving time perception intact. Conversely, inactivation of the FM-FM area impairs the bat's ability to detect small differences in the time of arrival of two echoes, while leaving frequency perception unchanged.
Investigation of this auditory system was greatly facilitated by knowledge of the stimuli relevant to bats. It remains to be seen whether these cortical areas are functionally or anatomically analogous to particular fields in cats, monkeys, and humans. Regardless, ethologically significant stimuli are likely to be as useful in studying these other species as they have been in studies of bats.
A Second Sound-Localization Pathway from the Inferior Colliculus Involves the Cerebral Cortex in Gaze Control
Many auditory neurons in the cerebral cortex are sensitive to interaural time and level differences and therefore to the location of sounds in space. Most of these cells have large receptive fields and broad tuning. In contrast to the auditory relays in the midbrain, however, there is no evidence for an organized spatial map of sound in any of the cortical areas sensitive to sound location.
The sound-localization pathways in the cortex originate in the central nucleus of the inferior colliculus and ascend through the auditory thalamus, area A1, and cortical association areas, eventually reaching the frontal eye fields involved in gaze control. Eye or head movements can be elicited by stimulating the frontal eye fields, which connect directly to brain stem tegmentum premotor nuclei that mediate gaze changes, as well as to the superior colliculus. But the midbrain pathway from location-sensitive neurons in the inferior colliculus to the superior colliculus to gaze-control circuitry can directly regulate orientation movements of the head, eyes, and ears. Why should there be a second sound-localization pathway connected to gaze-control circuitry?
Behavioral experiments shed light on this question. Although lesions of A1 can result in profound sound-localization deficits in a monkey, no deficiency is seen when the task is simply to indicate the side of the sound source by pushing a lever. The deficit becomes apparent only when the animal must approach the location of a brief sound source, that is, when the task is the more complex one of forming an image of the source, remembering it, and moving toward it.
Experiments in barn owls have produced particularly compelling evidence. The ability of owls to orient to sounds in space is unaffected by inactivation of the avian equivalent of the frontal eye fields. Similarly, when the midbrain localization pathway is disrupted by pharmacological inactivation of the superior colliculus, the probability of an accurate head turn is decreased but animals still respond correctly more than half of the time. In contrast, when both structures are inactivated, animals are completely unable to orient accurately to acoustic stimuli on the contralateral side. Thus cortical and subcortical sound-localization pathways have parallel access to gaze control centers, perhaps providing some redundancy. Moreover, when only the frontal eye fields are inactivated, birds lose their ability to orient their gaze toward a target that has been extinguished and must be remembered, just as is seen with mammalian A1 lesions. Thus in both mammals and birds cortical pathways are required for more complex sound-localization tasks.
This appears to be a general difference between cortical and subcortical pathways. Subcortical circuits are important for rapid and reliable performance of behaviors that are critical to survival. Cortical circuitry allows for working memory, complex recognition tasks, and selection of stimuli and evaluation of their significance, resulting in slower but more differentiated performance. Examples of this also exist in auditory pathways not involved in localization. Conditioned fear responses to simple auditory stimuli are mediated by direct rapid pathways from the auditory thalamus to the amygdala; they can be elicited after cortical inactivation. However, fear responses that require more complex discrimination of auditory stimuli require pathways through the cortex, and are accordingly slower but more specific.
Auditory Circuits in the Cerebral Cortex Are Segregated into Separate Processing Streams
In the visual system the output from the primary visual cortex is segregated into separate dorsal and ventral streams concerned respectively with object location in space and object identification. A similar division of labor is thought to exist in the somatosensory cortex, and recent evidence suggests that the auditory cortex follows this plan.
Anatomical tracing studies of the three most accessible belt areas in primates show that the more rostral and ventral areas connect primarily to the more rostral and ventral areas of the temporal lobe, whereas the more caudal area projects to the dorsal and caudal temporal lobe. In addition, these belt areas and their temporal lobe targets both project to largely different areas of the frontal lobes (Figure 31–13).
The "what" and "where" streams in the auditory cortical system of primates.
The ventral "what" stream and dorsal "where" stream originate in different parts of primary and belt cortex and ultimately project to distinct regions of prefrontal cortex through independent paths. (MGB, medial geniculate body of the thalamus; PB, parabelt cortex; PFC, prefrontal cortex; PP, posterior parietal cortex; T2/T3, areas of temporal cortex.) (Modified, with permission, from Rauschecker 2000 and from Romanski and Averbeck 2009.)
The frontal areas receiving anterior auditory projections are generally implicated in nonspatial functions, whereas those that are targets of posterior auditory areas are implicated in spatial processing. Electrophysiological and imaging studies provide support for this. Caudal and parietal areas are more active when a sound must be located or moves, and ventral areas are more active during identification of the same stimulus or analysis of its pitch. Consistent with this segregation, inactivation of the posterior auditory field in cats impairs performance of a sound-localization task, whereas inactivation of the anterior auditory field interferes with a pattern-discrimination task, but not vice versa. Thus anterior-ventral pathways may identify auditory objects by analyzing spectral and temporal characteristics of sounds, whereas the more dorsal-posterior pathways may specialize in sound-source location, detection of sound-source motion, and spatial segregation of sources.
Although the idea that all sensory areas of the cerebral cortex initially segregate object identification and location is attractive, it is likely an oversimplification. It is clear that the medial-belt areas of the auditory cortex project to both dorsal and ventral frontal cortices, and neurons with broad spatial responsiveness are distributed throughout caudal and anterior areas. Imaging studies with more complex stimuli suggest that parietal pathways are involved in additional functions, including analysis of the temporal properties of acoustic stimuli such as spectral motion. The latter property might explain the clear role of the posterior pathway in speech perception in humans. Nonetheless, although the details may differ between systems, the basic concept holds that sensory systems decompose stimuli into features and analyze these in discrete pathways.
The Cerebral Cortex Modulates Processing in Subcortical Auditory Areas
An intriguing feature of all mammalian cortical areas, and one shared by the auditory system, is the massive projection from the cortex back to lower areas. There are almost 10-fold as many corticofugal fibers entering the sensory thalamus as there are axons projecting from the thalamus to the cortex. Projections from the auditory cortex also innervate the inferior colliculus, olivocochlear neurons, some basal ganglionic structures, and even the dorsal cochlear nucleus.
Insights into possible functions of this feedback have come from the bat's auditory system. Silencing of frequency-specific cortical areas leads to decreased thalamic and collicular responses, whereas activation of cortical projections increases and sharpens the responses of some neurons. The auditory cortex can therefore actively adjust and improve auditory signal processing in subcortical structures.
A variety of evidence suggests that cortical feedback also occurs in the visual and somatosensory components of the thalamus. This challenges the view that ascending sensory pathways are purely feedforward circuits, and suggests that we should regard the thalamus and cortex as reciprocally and highly interconnected circuits in which the cortex exercises some top-down control of perception.