Severe and extensive neonatal hearing loss in cats results in auditory cortex plasticity that differentiates into two regions.

We examined the response characteristics of primary auditory cortex (A1) neurons in adult cats partially but extensively deafened by ototoxic drugs 2-8 days after birth. The damage evoked extensive A1 topographic map reorganization as also found by others, but a novel finding was that in the majority of cats with low-frequency edges to the cochlear lesion, the area of reorganization segregated into two areas expressing the same novel frequency inputs but differentiated by neuronal sensitivity and responsiveness. Immediately adjacent to normal A1 is an approximately 1.2-mm-wide area of reorganization in which sensitivity and responsiveness to sound are similar to that in normal A1 in the same animals and in unlesioned adult animals. Extending further into deprived A1 is a more extensive area of reorganization where neurons have poorer sensitivity and responsiveness to new inputs. These two areas did not differ in response-area bandwidth and response latency. We interpret these novel changes as the cortical consequences of severe receptor organ lesions extending to low-frequency cochlear regions. We speculate that the two areas of A1 reorganization may reflect differences in the transcortical spatial distribution of thalamo-cortical and horizontal intracortical connections. Qualitatively similar changes in response properties have been seen after retinal lesions producing large areas of visual cortical reorganization, suggesting they might be a general consequence of receptor lesions that deprive large regions of cortex of normal input. These effects may have perceptual implications for the use of cochlear implants in patients with residual low-frequency hearing.

Mechanisms underlying the sensitivity of neurons in the lateral superior olive to interaural intensity differences.

The initial processing of interaural intensity differences (IIDs), the major cue to the azimuthal location of high-frequency sounds in mammals, is carried out by neurons in the lateral superior olivary nucleus (LSO) that receive excitatory input from the ipsilateral ear and inhibitory input from the contralateral ear (IE neurons). The "latency" hypothesis asserts that it is the effects of intensity differences on the latency, and hence the relative timing, of the synaptic inputs to these neurons that is the basis of their sensitivity to IIDs, while other models assign the major role to changes in the relative amplitude of the inputs. To test the latency hypothesis and to determine the contributions of changes in the relative timing and amplitude of synaptic inputs to the IID sensitivity of LSO neurons, a method was developed of generating sets of stimuli that produced either the same changes in the relative timing of inputs without any change in their amplitude (equivalent interaural time difference stimuli) or the same differences in amplitude without any difference in timing (delay-cancelled IID stimuli) as a given range of IIDs. Data were obtained from a sample of IE neurons in the LSO of anesthetized rats using these stimulus paradigms and click and tone-burst stimuli. For click stimuli, the IID sensitivity of a small proportion of neurons was explained entirely by sensitivity to differences in input timing, but the sensitivity of most neurons reflected either sensitivity to the relative amplitude of inputs or to the joint operation of both factors. In neurons whose sensitivity was tested at a number of different absolute sound pressure levels (SPLs), the relative contributions of the two factors tended to differ at different SPLs. The IID sensitivity of onset responses to tone stimuli could be classified into the same three categories but was explained for a larger proportion of neurons by sensitivity to differences in input timing. The IID sensitivity of the late response component of neurons with sustained responses to tones in all cases reflected sensitivity to the relative amplitude of the inputs. The results confirm the contribution of changes in latency produced by intensity changes to the IID sensitivity of the onset responses of many IE neurons in LSO but require rejection of the strong form of the latency hypothesis, which asserts that this factor alone accounts for such sensitivity.

Injury- and use-related plasticity in adult auditory cortex.

After restricted cochlear lesions in adult animals the frequency selectivity of neurons in the cortical region deprived of its normal input by the lesion is changed such that the region is occupied by expanded representations of adjacent (perilesion) frequencies. These changes reflect a dynamic process of reorganization (plasticity) and are not explicable as passive consequences of the lesion. Analogous plasticity of cortical frequency selectivity and organization is seen following behavioural training that enhances the significance of particular acoustic stimuli. The occurrence of injury- and use-related auditory cortical plasticity gives rise to a number of questions relating to the mechanisms involved, the perceptual consequences and functional significance of such plastic changes, and their implications for the central processing of input from prosthetic devices. Evidence relating to these issues is briefly summarized in this review, and the directions of future research are considered.

Auditory laterality and attentional deficits after thalamic haemorrhage.

Thalamic lesions have been shown to produce severe cognitive deficits involving language and memory. A majority of the studies have reported cognitive deficits after lesions in the anterior and dorsomedial thalamic nuclei. We report five case studies of effects on language processing after postero-dorsal thalamic haemorrhages. Four of the patients had lesions on the right side, and one patient had a lesion on the left side. Effects on language processing were investigated with the dichotic listening test with consonant-vowel syllables. This test, in which conflicting auditory stimuli are presented simultaneously to the two ears, has been used to probe differences in language processing in the left and right hemispheres. The four patients with right-sided lesions reported almost none of the syllables presented to the left ear, and were unable to modify this massive right ear advantage by directing attention to the left or right ear. The patient with a left-sided lesion showed a weaker left ear advantage, and was able to modify his responses by shifting attention, to an extent similar to that of healthy reference individuals. When tested with monaural stimulus presentation, the scores of all patients rose to almost 100% correct for each ear. The pattern of effects with dichotic stimuli under different instructional conditions cannot be accounted for in purely structural terms, and indicates that lesions in the posterior part of the thalamus, including the pulvinar nucleus and medial geniculate body, produce deficits not only in processing of complex auditory stimuli but also in the allocation of attention to input from one ear or the other.

Injury- and use-related plasticity in the adult auditory system.

After restricted cochlear lesions in adult animals, the frequency selectivity of neurons in the cortical region deprived of its normal input by the lesion is changed such that the region is occupied by expanded representations of adjacent (perilesion) frequencies. Analogous changes in cortical frequency selectivity and organization are seen as a consequence of behavioral training that enhances the significance of particular acoustic stimuli. The occurrence of such reorganization in a wide range of species (including simian primates) suggests that it would also occur in humans. Direct evidence in support of this suggestion is provided by a small body of functional imaging evidence. Although such reorganization almost certainly does not have a compensatory function, such a profound change in the pattern of cortical activation produced by stimuli exciting perilesion parts of the receptor epithelium would be expected to have perceptual consequences and, perhaps, clinical implications.

Injury-induced reorganization in adult auditory cortex and its perceptual consequences.

Restricted cochlear lesions in adult animals result in a reorganization of auditory cortex such that the cortical region deprived of its normal input by the lesion is occupied by expanded representations of adjacent cochlear loci, and thus of the frequencies represented at those loci. Analogous injury-induced reorganization is seen in somatosensory, visual and motor cortices of adult animals after restricted peripheral lesions. The occurrence of such reorganization in a wide range of species (including simian primates), and across different sensory systems and forms of peripheral lesion, suggests that it would also occur in humans with similar lesions. Direct evidence in support of this suggestion is provided by a small body of functional imaging evidence in the somatosensory and auditory systems. Although such reorganization does not seem to have a compensatory function, such a profound change in the pattern of cortical activation produced by stimuli exciting peri-lesion parts of the receptor epithelium would be expected to have perceptual consequences. However, there is only limited psychophysical evidence for perceptual effects that might be attributable to injury-induced cortical reorganization, and very little direct evidence for the correlation between the perceptual phenomena and the occurrence of reorganization.

Specificity of perceptual learning in a frequency discrimination task.

On a variety of visual tasks, improvement in perceptual discrimination with practice (perceptual learning) has been found to be specific to features of the training stimulus, including retinal location. This specificity has been interpreted as evidence that the learning reflects changes in neuronal tuning at relatively early processing stages. The aim of the present study was to examine the frequency specificity of human auditory perceptual learning in a frequency discrimination task. Difference limens for frequency (DLFs) were determined at 5 and 8 kHz, using a three-alternative forced choice method, for two groups of eight subjects before and after extensive training at one or the other frequency. Both groups showed substantial improvement at the training frequency, and much of this improvement generalized to the nontrained frequency. However, a small but statistically significant component of the improvement was specific to the training frequency. Whether this specificity reflects changes in neural frequency tuning or attentional changes remains unclear.

Absence of plasticity of the frequency map in dorsal cochlear nucleus of adult cats after unilateral partial cochlear lesions.

In adult animals, lesions to parts of the auditory receptor organ, the cochlea, can produce plasticity of the topographic (cochleotopic) frequency map in primary auditory cortex and a restricted or patchy plasticity in the auditory midbrain. This effect is similar to the plasticity of topographic maps of the sensory surface seen in visual and somatosensory cortices after restricted damage to the appropriate receptor surface in these sensory systems. There is dispute about the extent to which subcortical effects contribute to cortical plasticity. Here, we have examined whether topographic map plasticity similar to that seen in the auditory cortex and the midbrain is observed in the adult auditory brainstem. When partial cochlear lesions were produced in the same manner as those that were produced in the cortex and midbrain studies, we found no plasticity of the frequency map in the dorsal cochlear nucleus (DCN). Small regions of the DCN that were deprived of their normal, most sensitive frequency (characteristic frequency; CF) input by the cochlear lesion appeared to have acquired new CFs at frequencies at or near the edge of the cochlear lesion. However, examination of thresholds at the new CFs established that the changes simply reflected the residue of prelesion input to those sites: The patterns of CF thresholds were very well predicted by simple calculations of the patterns that were expected from such residual input. The results of this study suggest that the DCN does not exhibit the type of plasticity that has been found in the auditory cortex and midbrain; therefore, it does not account for the changes in responsiveness observed in the higher level structures under similar experimental conditions.

Functional specialization in auditory cortex: responses to frequency-modulated stimuli in the cat's posterior auditory field.

The mammalian auditory cortex contains multiple fields but their functional role is poorly understood. Here we examine the responses of single neurons in the posterior auditory field (P) of barbiturate- and ketamine-anesthetized cats to frequency-modulated (FM) sweeps. FM sweeps traversed the excitatory response area of the neuron under study, and FM direction and the linear rate of change of frequency (RCF) were varied systematically. In some neurons, sweeps of different sound pressure levels (SPLs) also were tested. The response magnitude (number of spikes corrected for spontaneous activity) of nearly all field P neurons varied with RCF. RCF response functions displayed a variety of shapes, but most functions were of low-pass characteristic or peaked at rather low RCFs (<100 kHz/s). Neurons with strong responses to high RCFs (high-pass or nonselective RCF response function characteristics) all displayed spike count-SPL functions to tone burst onsets that were monotonic or weakly nonmonotonic. RCF response functions and best RCFs often changed with SPL. For most neurons, FM directional sensitivity, quantified by a directional sensitivity (DS) index, also varied with RCF and SPL, but the mean and width of the distribution of DS indices across all neurons was independent of RCF. Analysis of response timing revealed that the phasic response of a neuron is triggered when the instantaneous frequency of the sweep reaches a particular value, the effective Fi. For a given neuron, values of effective Fi were independent of RCF, but depended on FM direction and SPL and were associated closely with the boundaries of the neuron's frequency versus amplitude response area. The standard deviation (SD) of the latency of the first spike of the response decreased with RCF. When SD was expressed relative to the rate of change of stimulus frequency, the resulting index of frequency jitter increased with RCF and did so rather uniformly in all neurons and largely independent of SPL. These properties suggest that many FM parameters are represented by, and may be encoded in, orderly temporal patterns across different neurons in addition to the strength of responses. When compared with neurons in primary and anterior auditory fields, field P neurons respond better to relatively slow FMs. Together with previous studies of responses to modulations of amplitude, such as tone onsets, our findings suggest more generally that field P may be best suited for processing signals that vary relatively slowly over time.

The posterior field P of cat auditory cortex: coding of envelope transients.

The posterior field (P) of the cat auditory cortex contains a very high proportion of neurons whose responses change non-monotonically with the sound pressure level (SPL) of tonal stimuli, leading to circumscribed frequency-SPL response areas, and it has therefore been suggested that field P may be specialized for processing of sound intensity. We demonstrate here a great diversity of response areas in field P. Furthermore, by varying tone SPL and rise time, we show that, as in primary auditory cortex (AI), the onset response of a field P neuron is better described as a function of the instantaneous peak pressure (envelope) at the time of response generation than of the steady-state SPL of the stimulus. Such responses could be used to track transients or represent envelopes in more general terms, rather than to code SPL. Compared with AI, field P neurons have relatively long minimum latencies along with a large jitter in spike timing. Tracking would therefore be most effective for slowly varying envelopes, and one function of the inhibition that generates non-monotonicity in field P may be to suppress temporally sluggish responses to rapid transients, such as the onsets of high-SPL, short rise time tones. Field P may thus be specialized for coding slowly varying signals.

Neuronal responses across cortical field A1 in plasticity induced by peripheral auditory organ damage.

The adult auditory cortex is capable of a plastic reorganization of its tonotopic map after damage to restricted parts of the cochlear sensory epithelium. We examine the precise conditions of cochlear damage required to demonstrate such plasticity in the primary auditory cortex (A1) of the cat and the changes observed in neuronal responses in the A1 which has reorganized in plasticity of the tonotopic map. From these data we attempt to predict the conditions required for similar plasticity to occur in humans after cochlear damage.

Loudness perception and frequency discrimination in subjects with steeply sloping hearing loss: possible correlates of neural plasticity.

Loudness functions and frequency difference limens (DLFs) were measured in five subjects with steeply sloping high-frequency sensorineural hearing loss. The stimuli were pulsed pure tones encompassing a range of frequencies. Loudness data were obtained using a 2AFC matching procedure with a 500-Hz reference presented at a number of levels. DLFs were measured using a 3AFC procedure with intensities randomized within 6 dB around an equal-loudness level. Results showed significantly shallower loudness functions near the cutoff frequency of the loss than at a lower frequency, where hearing thresholds were near normal. DLFs were elevated, on average, relative to DLFs measured using the same procedure in five normally hearing subjects, but showed a local reduction near the cutoff frequency in most subjects with high-frequency loss. The loudness data are generally consistent with recent models that describe loudness perception in terms of peripheral excitation patterns that are presumably restricted by a steeply sloping hearing loss. However, the DLF data are interpreted with reference to animal experiments that have shown reorganization in the auditory cortex following the introduction of restricted cochlear lesions. Such reorganization results in an increase in the spatial representation of lesion-edge frequencies, and is comparable with the functional reorganization observed in animals following frequency-discrimination training. It is suggested that similar effects may occur in humans with steeply sloping high-frequency hearing loss, and therefore, the local reduction in DLFs in our data may reflect neural plasticity.

First-spike timing of auditory-nerve fibers and comparison with auditory cortex.

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.

Injury-induced reorganization of frequency maps in adult auditory cortex: the role of unmasking of normally-inhibited inputs.

Restricted cochlear lesions in adult animals, causing partial deafness, result in a reorganization of primary auditory cortex (AI) such that the region deprived of its normal input by the lesion is occupied by an expanded representation of peri-lesion cochlear regions, and hence of peri-lesion frequencies. One possible mechanism underlying the change in frequency responsiveness involved in such reorganization is that inputs to the cortical neurons at frequencies at and near their "new" post-lesion characteristic frequencies (CFs) are normally present but suppressed by inhibition, and are "unmasked" by the effects of the lesion. Evidence in support of this explanation is provided by two-tone forward-masking experiments which reveal that many AI neurons receive surround inhibitory input. When input to such neurons at their CF is reduced by an intense temporary-threshold-shift (TTS)-inducing stimulus, the response areas of some neurons expand into the region of their inhibitory surrounds, the effect that would be expected if unmasking were involved in cortical reorganization. In other neurons, however, response areas contracted after the TTS-inducing stimulation. Although unmasking of normally-inhibited inputs is likely to contribute to auditory cortical reorganization, the immediate unmasking that is seen in visual and somatosensory systems is unlikely to play a major role in auditory cortical reorganization, as no evidence of immediate unmasking was seen following acute cochlear lesions in guinea pigs.

On determinants of first-spike latency in auditory cortex.

The first-spike latency of neurones at any level of the auditory pathway decreases with stimulus amplitude. As stimuli are generally shaped with rise functions to avoid spectral splatter, a common interpretation of the latency decrease is that the amplitude of the signal reaches the neurone's firing threshold earlier during the rise time. We demonstrate here, for auditory cortex neurones and by varying the amplitude and rise time of tonal stimuli, that this threshold model is inadequate to account for the observed latency changes, particularly when adaptive processes are taken into account. The data raise the possibility that latency may be a function of other properties associated with a signal's onset, such as rate of change of peak pressure.

Injury- and use-related plasticity in the primary sensory cortex of adult mammals: possible relationship to perceptual learning.

1. Restricted cochlear lesions in adult animals result in a reorganization of auditory cortex such that the cortical region deprived of its normal input by the lesion is occupied by expanded representations of adjacent cochlear loci (and thus of the frequencies represented at those loci). Analogous injury-induced reorganization is seen in somatosensory, visual and motor cortices of adult animals after restricted peripheral lesions. 2. Rather than constituting a central compensation for the peripheral loss, such reorganization appears to be an extreme form of changes in cortical organization that occur as a consequence of altered patterns of input such as arise from differential use of restricted regions of receptor surfaces ('use-related' reorganization). Thus, the frequency organization of auditory cortex is modified in animals trained to perform a frequency discrimination task and analogous changes in the frequency selectivity of cortical neurons are produced by classical conditioning procedures. 3. Recent evidence from the visual system suggests that changes similar to those involved in injury- and use-related cortical reorganization may underlie some forms of what has been called 'perceptual learning', the improvement in sensory/ perceptual discriminative performance with practice. Some forms of such learning are highly specific to the particular stimuli used in training (i.e. do not generalize to other stimuli), suggesting that the improved performance reflects a change in neural circuitry at a relatively early level of sensory processing. The limited available evidence supports the occurrence of such learning in the auditory system. 4. Recent studies using functional imaging and related techniques indicate that injury- and use-related reorganization occurs in human sensory and motor cortex.

Sensitivity to interaural intensity differences of neurons in primary auditory cortex of the cat. I. types of sensitivity and effects of variations in sound pressure level.

1. Interaural intensity differences (IIDs) provide the major cue to the azimuthal location of high-frequency narrowband sounds. In recent studies of the azimuthal sensitivity of high-frequency neurons in the primary auditory cortex (field AI) of the cat, a number of different types of azimuthal sensitivity have been described and the azimuthal sensitivity of many neurons was found to vary as a function of changes in stimulus intensity. The extent to which the shape and the intensity dependence of the azimuthal sensitivity of AI neurons reflects features of their IID sensitivity was investigated by obtaining data on IID sensitivity from a large sample of neurons with a characteristic frequency (CF) > 5.5 kHz in AI of anesthetized cats. IID sensitivity functions were classified in a manner that facilitated comparison with previously obtained data on azimuthal sensitivity, and the effects of changes in the base intensity at which IIDs were introduced were examined. 2. IID sensitivity functions for CF tonal stimuli were obtained at one or more intensities for a total of 294 neurons, in most cases by a method of generating IIDs that kept the average binaural intensity (ABI) of the stimuli at the two ears constant. In the standard ABI range at which a function was obtained for each unit, five types of IID sensitivity were distinguished. Contra-max neurons (50% of the sample) had maximum response (a peak or a plateau) at IIDs corresponding to contralateral azimuths, whereas ipsi-max neurons (17%) had the mirror-image form of sensitivity. Near-zero-max neurons (18%) had a clearly defined maximum response (peak) in the range of +/- 10 dB IID, whereas a small group of tough neurons (2%) had a restricted range of minimal responsiveness with near-maximal responses at IIDs on either side. A final 18% of AI neurons were classified as insensitive to IIDs. The proportions of neurons exhibiting the various types of sensitivity corresponded closely to the proportions found to exhibit corresponding types of azimuthal sensitivity in a previous study. 3. There was a strong correlation between a neuron's binaural interaction characteristics and the form of its IID sensitivity function. Thus, neurons excited by monaural stimulation of only one ear but with either inhibitory, facilitatory, or mixed facilitatory-inhibitory effects of stimulation of the other ear had predominantly contra-max IID sensitivity (if contralateral monaural stimulation was excitatory) or ipsi-max sensitivity (if ipsilateral monaural stimulation was excitatory). Neurons driven weakly or not at all by monaural stimulation but facilitated binaurally almost all exhibited near-zero-max IID sensitivity. The exception to this tight association between binaural input and IID sensitivity was provided by neurons excited by monaural stimulation of either ear (EE neurons). Although EE neurons have frequently been considered to be insensitive to IIDs, our data were in agreement with two recent reports indicating that they can exhibit various forms of IID sensitivity: only 23 of 75 EE neurons were classified as insensitive and the remainder exhibited diverse types of sensitivity. 4. IID sensitivity was examined at two or more intensities (3-5 in most cases) for 84 neurons. The form of the IID sensitivity function (defined in terms of both shape and position along the IID axis) was invariant with changes in ABI for only a small proportion of IID-sensitive neurons (approximately 15% if a strict criterion of invariance was employed), and for many of these neurons the spike counts associated with a given IID varied with ABI, particularly at near-threshold levels. When the patterns of variation in the form of IID sensitivity produced by changes in ABI were classified in a manner equivalent to that used previously to classify the effects of intensity on azimuthal sensitivity, there was a close correspondence between the effects of intensity on corresponding types of azimuthal and IID sensitivity

Responses of neurons in the inferior colliculus of the rat to interaural time and intensity differences in transient stimuli: Implications for the latency hypotheses.

Although the sensitivity to interaural intensity differences (IIDs) of neurons receiving excitatory - inhibitory binaural input (EI neurons) has been examined in numerous studies, the mechanisms underlying this sensitivity remain unclear. According to the 'latency hypotheses' neuronal sensitivity to IIDs reflects sensitivity to differences in the timing of ipsilateral and contralateral inputs that are produced as a consequence of the effects of intensity upon latency. If the latency hypothesis is correct, a neuron's responses over any given IID range should be predicted by its responses to the interaural time differences (ITDs) that are 'equivalent' to the IIDs tested, in the sense that they produce the same changes in the relative timing of inputs. This prediction from the latency hypotheses were examined by determining the sensitivity of EI neurons in the inferior colliculus of anesthetized rats to IIDs and ITDs in click stimuli, under conditions that allowed 'equivalent' ITDs to be estimated. In approximately 10% of the 41 neurons tested, the IID-sensitivity function was a perfect or near-perfect match to the equivalent-ITD function, indicating that IID sensitivity could be entirely accounted for in terms of sensitivity to intensity-produced neural time differences, as asserted by the latency hypothesis. For the majority of neurons, however, sensitivity to equivalent ITDs accounted only partially for the characteristics of the IID-sensitivity function; other features of the function in these cases appeared to reflect the operation of an additional factor, most probably the relative magnitude of the inputs from the two ears. Although the conclusions are qualified by the fact that one of the assumptions on which the estimation of equivalent ITDs was based was probably not satisfied for some neurons, the results suggest that intensity-produced changes in both the magnitude and the timing of excitatory and inhibitory inputs shape the IID sensitivity of most EI neurons.

Topographic representation of tone intensity along the isofrequency axis of cat primary auditory cortex.

The sound pressure level (SPL), henceforth termed intensity, of acoustic signals is encoded in the central auditory system by neurons with different forms of intensity sensitivity. However, knowledge about the topographic organization of neurons with these different properties and hence about the spatial representation of intensity, especially at higher levels of the auditory pathway, is limited. Here we show that in the tonotopically organized primary auditory cortex (AI) of the cat there are orderly topographic organizations, along the isofrequency axis, of several neuronal properties related to the coding of the intensity of tones, viz. minimum threshold, dynamic range, best SPL, and non-monotonicity of spike count--intensity functions to tones of characteristic frequency (CF). Minimum threshold, dynamic range, and best SPL are correlated and alter periodically along isofrequency strips. The steepness of the high-intensity descending slope of spike count--intensity functions also varies systematically, with steepest slopes occurring in the regions along an isofrequency strip where low thresholds, narrow dynamic ranges and low best SPLs are found. As a consequence, CF-tones of various intensities are represented by orderly and, for most intensities, periodic, spatial patterns of distributed neuronal activity along an isofrequency strip. For low--to--moderate intensities, the mean relative activity along the entire isofrequency strip increases rapidly with intensity, with the spatial pattern of activity remaining quite constant along the strip. At higher intensities, however, the mean relative activity along the strip remains fairly constant with changes in intensity, but the spatial patterns change markedly. As a consequence of these effects, low- and high-intensity tones are represented by complementary distributions of activity alternating along an isofrequency strip. We conclude that in AI tone intensity is represented by two complementary modes, viz. discharge rate and place. Furthermore, the magnitude of the overall changes in the representation of tone intensity in AI appears to be closely related to psychophysical measures of loudness and of intensity discrimination.

Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex.

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.