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

Abstract

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.

Neural Correlates of an Auditory Afterimage in Primary Auditory Cortex

“…The authors suggested that the CF of neurons corresponding to the notch had shifted toward the edge frequencies of the notch so that fewer neurons could respond to the probe tone. These proposed central changes in tonotopic organization induced by a NN are supposed to be similar to those following cochlear damage (Rajan et al 1993). The results of Pantev et al (1999) then corroborate the assumption that long-lasting presentation of a NN induces a ''functional deafferentation.…”

The mechanisms of tinnitus: Perspectives from human functional neuroimaging

“…A maladaptive response to this loss of input causes expansion of the tonotopic map so that this affected portion now becomes responsive to the adjacent frequency at which hearing threshold is normal -the lesion-edge frequency ( Figure 7). Of relevance for human neuroimaging studies, animal research has shown that a restricted cochlear lesion in adult animals drives neuroplastic changes in the frequency gradient within primary auditory cortex (Robertson and Irvine, 1989;Kaas, 1991, Rajan et al, 1993Schwaber et al 1993;Irvine et al, 2001). One theory of TI proposes that it is a consequence of such cortical reorganisation (e.g., Salvi et al, 2000a).…”

Residual Inhibition Functions Overlap Tinnitus Spectra and the Region of Auditory Threshold Shift

“…Although the specific role of hearing loss is debated (see Weisz et al 2006), most cases of tinnitus are accompanied by hearing impairment associated with noise exposure or the aging process. One consequence of hearing loss identified by studies of animals exposed to noise trauma is a reorganization of the tonotopic map in primary auditory cortex (A1), such that sound frequencies near the edge of the cortical region of normal hearing come to be over-represented at the expense of sound frequencies in the region affected by hearing impairment (Robertson and Irvine 1989;Harrison et al 1991;Rajan et al 1993;Eggermont and Komiya 2000). It has been proposed that this overrepresentation of edge frequencies corresponds to the tinnitus sensation (see Rauschecker 1999, for a review).…”