In several sensory systems, the conversion of the representation of stimuli from graded membrane potentials into stochastic spike trains is performed by ribbon synapses. In the mammalian auditory system, the spiking characteristics of the vast majority of primary afferent auditory-nerve (AN) fibers are determined primarily by a single ribbon synapse in a single inner hair cell (IHC), and thus provide a unique window into the operation of the synapse. Here, we examine the distributions of interspike intervals (ISIs) of cat AN fibers under conditions when the IHC membrane potential can be considered constant and the processes generating AN fiber activity can be considered stationary, namely in the absence of auditory stimulation. Such spontaneous activity is commonly thought to result from an excitatory Poisson point process modified by the refractory properties of the fiber, but here we show that this cannot be the case. Rather, the ISI distributions are one to two orders of magnitude better and very accurately described as a result of a homogeneous stochastic process of excitation (transmitter release events) in which the distribution of interevent times is a mixture of an exponential and a gamma distribution with shape factor 2, both with the same scale parameter. Whereas the scale parameter varies across fibers, the proportions of exponentially and gamma distributed intervals in the mixture, and the refractory properties, can be considered constant. This suggests that all of the ribbon synapses operate in a similar manner, possibly just at different rates. Our findings also constitute an essential step toward a better understanding of the spike-train representation of time-varying stimuli initiated at this synapse, and thus of the fundamentals of temporal coding in the auditory pathway.

The aim of this study was to determine whether auditory perceptual learning is associated with changes in the frequency organization and/or neuronal response properties of primary auditory cortex (AI). Five out of six cats trained on an 8 kHz frequency discrimination task showed improvements in performance that reflected changes in discriminative capacity. Quantitative measures of the response characteristics and frequency organization of AI revealed that the frequency organization of AI in trained cats did not differ from that in controls, but there was a tendency for neurons with a CF immediately above 8 kHz to have slightly broader tuning in the trained cats than in controls, and neurons in one of these bands had significantly shorter latency. These results are in accord with recent reports that cortical topography in primary visual cortex is unchanged in animals trained on visual discrimination tasks, but are at variance with an earlier report of enlarged representations of training frequencies in AI of monkeys trained on a frequency discrimination task. It is concluded that substantial changes in perceptual discriminative capacity can occur without change in primary cortical topography and with only small changes in neuronal response characteristics.

To investigate subcortical contributions to cortical reorganization, the frequency organization of the ventral nucleus of the medial geniculate body (MGv) in six normal adult cats and in eight cats with restricted unilateral cochlear lesions was investigated using multiunit electrophysiological recording techniques. The tonotopic organization of MGv in the lesioned animals, with severe mid-to-high frequency hearing losses, was investigated 40-186 days following the lesioning procedure. Frequency maps were generated from neural responses to pure tone bursts presented separately to each ear under barbiturate anesthesia. Consideration of the frequency organization in normal animals, and of the apparently normal representation of the ipsilateral (unlesioned) cochlea in lesioned animals, allowed for a detailed specification of the extent of changes observed in MGv. In the lesioned animals it was found that, in the region of MGv in which mid-to-high frequencies are normally represented, there was an "expanded representation" of lesion-edge frequencies. Neuron clusters within these regions of enlarged representation that had "new" characteristic frequencies displayed response properties (latency, bandwidth) very similar to those in normal animals. Thresholds of these neurons were not consistent with the argument that the changes merely reflect the residue of prelesion responses, suggesting a dynamic process of reorganization. The tonotopic reorganization observed in MGv is similar to that seen in the primary auditory cortex and is more extensive than the reorganization found in the auditory midbrain, suggesting that the auditory thalamus plays an important role in cortical plasticity.

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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.