We have examined the effect of restricted unilateral cochlear lesions on the orderly topographic mapping of sound frequency in the auditory cortex of adult guinea pigs. These lesions, although restricted in spatial extent, resulted in a variety of patterns of histological damage to receptor cells and nerve fibres within the cochlea. Nevertheless, all lesions resulted in permanent losses of sensitivity of the cochlear neural output across a limited frequency range. Thirty-five to 81 days after such damage to the organ of Corti, the area of contralateral auditory cortex in which the lesioned frequency range would normally have been represented was partly occupied by an expanded representation of sound frequencies adjacent to the frequency range damaged by the lesion. The thresholds at their new characteristic frequencies (CFs) of clusters of cortical neurones in these regions were close to normal thresholds at those frequencies (mean difference across all animals was 3.8 dB). In a second series of experiments, the responses of neurone clusters were examined within hours of making similar cochlear lesions. It was found that shifts in CF toward frequencies spared by the lesions could occur, but thresholds were greatly elevated compared to normal (mean difference was 31.7 dB in five animals). The emergence of sensitive drive in such regions after prolonged recovery periods in lesioned animals thus suggests that the auditory cortical frequency map undergoes reorganization in cases of partial deafness. Some features of this reorganization are similar to changes reported in somatosensory cortex after peripheral nerve injury, and this form of plasticity may therefore be a feature of all adult sensory systems.

We examined the effect of unilateral restricted cochlear lesions in adult cats on the topographic representations ("maps") of the lesioned and unlesioned cochleas in the primary auditory cortex (AI) contralateral to the lesioned cochlea. Frequency (tonotopic) maps were derived by conventional multineuron mapping procedures in anesthetized animals. In confirmation of a study in adult guinea pigs (Robertson and Irvine [1989] J. Comp. Neurol. 282:456-471), we found that 2-11 months after the unilateral cochlear lesion the map of the lesioned cochlea in the contralateral AI was altered so that the AI region in which frequencies with lesion-induced elevations in cochlear neural sensitivity would have been represented was occupied by an enlarged representation of lesion-edge frequencies (i.e., frequencies adjacent to those with elevated cochlear neural sensitivity). Along the tonotopic axis of AI the total representation of lesion-edge frequencies could extend up to approximately 2.6 mm rostal to the area of normal representation of these frequencies. There was no topographic order within this enlarged representation. Examination of threshold sensitivity at the characteristic frequency (CF, frequency to which the neurons were most sensitive) in the reorganized regions of the map of the lesioned cochlea established that the changes in the map reflected a plastic reorganization rather than simply reflecting the residue of prelesion input. In contrast to the change in the map of the lesioned contralateral cochlea, the map of the unlesioned ipsilateral cochlea did not differ from those in normal animals. Thus, in contrast to the normal very good congruency between ipsilateral and contralateral AI maps, in the lesioned animals ipsilateral and contralateral maps differed in the region of AI in which there had been a reorganization of the map of the lesioned cochlea. Outside the region of contralateral map reorganization, ipsilateral and contralateral AI maps remained congruent within normal limits. The difference between the two maps in the region of contralateral map reorganization suggested, in light of the physiology of binaural interactions in the auditory pathway, that the cortical reorganization reflected subcortical changes. Finally, response properties of neuronal clusters within the reorganized map of the lesioned cochlea were compared to normative data with respect to threshold sensitivity at CF, the size of frequency "response areas," and response latencies. In the majority of cases, CF thresholds were similar to normative data. The frequency "response areas" were slightly less sharply tuned than normal, but not significantly. Response latencies were significantly shorter than normal in three animals and significantly longer in one animal.

In natural environments that contain multiple sound sources, acoustic energy arising from the different sources sums to produce a single complex waveform at each of the listener's ears. The auditory system must segregate this waveform into distinct streams to permit identification of the objects from which the signals emanate [1]. Although the processes involved in stream segregation are now reasonably well understood [1, 2 and 3], little is known about the nature of our perception of complex auditory scenes. Here, we examined complex scene perception by having listeners detect a discrete change to an auditory scene comprising multiple concurrent naturalistic sounds. We found that listeners were remarkably poor at detecting the disappearance of an individual auditory object when listening to scenes containing more than four objects, but they performed near perfectly when their attention was directed to the identity of a potential change. In the absence of directed attention, this "change deafness" [4] was greater for objects arising from a common location in space than for objects separated in azimuth. Change deafness was also observed for changes in object location, suggesting that it may reflect a general effect of the dependence of human auditory perception on attention.

Electrical stimulation of spiral ganglion neurons in deafened cochlea, via a cochlear implant, provides a means of investigating the effects of the removal and subsequent restoration of afferent input on the functional organization of the primary auditory cortex (AI). We neonatally deafened seventeen cats before the onset of hearing, thereby abolishing virtually all afferent input from the auditory periphery. In seven animals, the auditory pathway was chronically reactivated with environmentallyderived electrical stimuli presented via a multi-channel intracochlear electrode array implanted at eight weeks of age. Electrical stimulation was provided by a clinical cochlear implant that was used continuously for periods of up to seven months. In ten long-term deafened cats and three age-matched normal hearing controls, an intracochlear electrode array was implanted immediately prior to cortical recording. We recorded from a total of 812 single unit and multi-unit clusters in AI of all cats as adults, using a combination of single tungsten and multi-channel silicon electrode arrays. The absence of afferent activity in the long-term deafened animals had little effect on the basic response properties of AI neurons but resulted in complete loss of the normal cochleotopic organization of AI. This effect was almost completely reversed by chronic reactivation of the auditory pathway via the cochlear implant. We hypothesize that maintenance or re-establishment of a cochleotopically organized AI by activation of a restricted sector of the cochlea -as demonstrated in the present study -contributes to the remarkable clinical performance observed among human patients implanted at a young age.

First-spike timing of auditory-nerve fibers and comparison with auditory cortex. J. Neurophysiol. 78: 2438-2454, 1997. The timing of the first spike of cat auditory-nerve (AN) fibers in response to onsets of characteristic frequency (CF) tone bursts was studied and compared with that of neurons in primary auditory cortex (AI), reported previously. Tones were shaped with cosine-squared rise functions, and rise time and sound pressure level were parametrically varied. Although measurement of first-spike latency of AN fibers was somewhat compromised by effects of spontaneous activity, latency was an invariant and inverse function of the maximum acceleration of peak pressure (i.e., a feature of the 2nd derivative of the stimulus envelope), as previously found in AI, rather than of tone level or rise time. Latency-acceleration functions of all AN fibers were of very similar shape, similar to that observed in AI. As in AI, latency-acceleration functions of different fibers were displaced along the latency axis, reflecting differences in minimum latency, and along the acceleration axis, reflecting differences in sensitivity to acceleration [neuronal transient sensitivity (S)]. S estimates increased with spontaneous rate (SR), but values of high-SR fibers exceeded those in AI. This suggests that S estimates are biased by SR per se, and that unbiased true S values would be less tightly correlated with response properties covarying with SR, such as firing threshold. S estimates varied with CF in a fashion similar to the cat's audiogram and, for low- and medium-SR fibers, matched those for AI neurons. Minimum latency decreased with increasing SR and CF. As in AI, the standard deviation of first-spike timing (SD) in AN was also an inverse function of maximum acceleration of peak pressure. The characteristics of the increase of SD with latency in a given AN fiber/AI neuron and across AN fibers/AI neurons revealed that the precision of first-spike timing to some stimuli can actually be higher in AI than in AN. The data suggest that the basic characteristics of the latency-acceleration functions of transient onset responses seen in cortex are generated at inner hair cell-AN fiber synapses. Implications for signal processing in the auditory system and for first-spike generation and adaptation in AN are discussed.