How Hearing Happens

Abstract

Research on the visual pathways has benefitted greatly from analysis at the single-cell level of human visual experience. This approach has contributed less to our grasp of auditory processing, for the greatest impact of audition lies in the comprehension of language, an attribute so specialized in humans that no satisfactory animal model exists. Higher auditory functions have nonetheless been successfully studied in three groups of animals for which sound analysis is of the utmost behavioral significance: owls, bats, and songbirds.Owls are nocturnal hunters of extraordinary auditory acuity. The barn owl, in particular, can track and strike its prey in total darkness. The neural substrate of the owl's ranging system is a map of auditory space on the avian homolog of the inferior colliculus. Synthesized from independent channels for the analysis of loudness and interaural time disparity, this emergent representation of auditory space permits an animal to localize targets with an accuracy in the horizontal plane of 1°. In the homolog of the superior colliculus, congruence of the auditory and visual maps of space is achieved during development by first constructing the latter representation and then superposing the former (Knudsen and Brainard 1991xKnudsen, E.I and Brainard, M.S. Science. 1991; 253: 85–87Crossref | PubMedSee all ReferencesKnudsen and Brainard 1991).Along with whales, bats are unique among mammals in their use of active echolocation. Rather than relying on sounds made by their prey, these animals emit acoustical pulses whose echoes bear information about the surroundings. The bat's auditory system has evolved alongside its vocalizations, so that the representation of sound in the cerebral cortex disproportionally emphasizes the frequencies and temporal characteristics of the animal's sounds and the corresponding echoes. The well-defined nature of the stimuli to which the bat is responsive has also facilitated analysis of auditory processing in this animal.The richness with which sound is represented in the bat's cerebral cortex rivals that of the primate's visual projection and displays a strikingly similar organization. The dominant theme is parallel processing: the bat's cortex is subdivided into at least nine areas, each of which conducts a particular type of analysis (reviewed bySuga 1990xSuga, N. Neural Networks. 1990; 3: 3–21Crossref | Scopus (134)See all ReferencesSuga 1990). The Doppler shift of an echo, for example, is represented in a huge array of neurons responsive to frequencies just above or below that of the chief vocal emission. This system provides the bat with a measure of the rate at which a target is approaching or receding. The timing of an echo is measured with a precision of microseconds by neurons that compare the onset of a sound pulse with that of the returning signal. This latency information informs the bat of the distance to an insect or to an inanimate object in the environment.As a form of learned vocal communication, bird song is the most accessible experimental model of human speech. The last of the accompanying articles, by D. Margoliash (1997 [this issue of Neuron]), reviews investigations of the bird's neural representation of song analysis and production. Even at the present, early stage in deciphering bird song, distinct parts of the system appear to be hierarchically organized to represent first complex song syllables, then their constituent tones. Among the most stimulating prospects for the next decade is the potential application of functional brain imaging to detect similar sequential representations of the phonemes and formants of human speech.