Unanesthetized Auditory Cortex Exhibits Multiple Codes for Gaps in Cochlear Implant Pulse Trains

Cochlear implant listeners receive auditory stimulation through amplitude-modulated electric pulse trains. Auditory nerve studies in animals demonstrate qualitatively different patterns of firing elicited by low versus high pulse rates, suggesting that stimulus pulse rate might influence the transmission of temporal information through the auditory pathway. We tested in awake guinea pigs the temporal acuity of auditory cortical neurons for gaps in cochlear implant pulse trains. Consistent with results using anesthetized conditions, temporal acuity improved with increasing pulse rates. Unlike the anesthetized condition, however, cortical neurons responded in the awake state to multiple distinct features of the gap-containing pulse trains, with the dominant features varying with stimulus pulse rate. Responses to the onset of the trailing pulse train (Trail-ON) provided the most sensitive gap detection at 1,017 and 4,069 pulse-per-second (pps) rates, particularly for short (25 ms) leading pulse trains. In contrast, under conditions of 254 pps rate and long (200 ms) leading pulse trains, a sizeable fraction of units demonstrated greater temporal acuity in the form of robust responses to the offsets of the leading pulse train (Lead-OFF). Finally, TONIC responses exhibited decrements in firing rate during gaps, but were rarely the most sensitive feature. Unlike results from anesthetized conditions, temporal acuity of the most sensitive units was nearly as sharp for brief as for long leading bursts. The differences in stimulus coding across pulse rates likely originate from pulse rate-dependent variations in adaptation in the auditory nerve. Two marked differences from responses to acoustic stimulation were: first, Trail-ON responses to 4,069 pps trains encoded substantially shorter gaps than have been observed with acoustic stimuli; and second, the Lead-OFF gap coding seen for <15 ms gaps in 254 pps stimuli is not seen in responses to sounds. The current results may help to explain why moderate pulse rates around 1,000 pps are favored by many cochlear implant listeners

Specialization for Sound Localization in Fields A1, DZ, and PAF of Cat Auditory Cortex

Cortical deactivation studies in cats have implicated the primary auditory cortex (A1), the dorsal zone (DZ), and the posterior auditory field (PAF) in sound localization behavior, and physiological studies in anesthetized conditions have demonstrated clear differences in spatial sensitivity among those areas. We trained cats to perform two listening tasks and then we recorded from cortical neurons in off-task and in both on-task conditions during single recording sessions. The results confirmed some of the results from anesthetized conditions and revealed unexpected differences. Neurons in each field showed a variety of firing patterns, including onset-only, complex onset and long latency, and suppression or offset. A substantial minority of units showed sharpening of spatial sensitivity, particularly that of onset responses, during task performance: 44 %, 35 %, and 31 % of units in areas A1, DZ, and PAF, respectively, showed significant spatial sharpening. Field DZ was distinguished by a larger percentage of neurons responding best to near-midline locations, whereas the spatial preferences of PAF neurons were distributed more uniformly throughout the contralateral hemifield. Those directional biases also were evident in measures of the accuracy with which neural spike patterns could signal sound locations. Field DZ provided the greatest accuracy for midline locations. The location dependence of accuracy in PAF was orthogonal to that of DZ, with the greatest accuracy for lateral locations. The results suggest a view of spatial representation in the auditory cortex in which DZ exhibits an overrepresentation of the frontal areas around the midline, whereas PAF provides a more uniform representation of contralateral space, including areas behind the head. Spatial preferences of area A1 neurons were intermediate between those of DZ and PAF, sharpening as needed for localization tasks

Abnormal Pitch Perception Produced by Cochlear Implant Stimulation

Contemporary cochlear implants with multiple electrode stimulation can produce good speech perception but poor music perception. Hindered by the lack of a gold standard to quantify electric pitch, relatively little is known about the nature and extent of the electric pitch abnormalities and their impact on cochlear implant performance. Here we overcame this obstacle by comparing acoustic and electric pitch perception in 3 unilateral cochlear-implant subjects who had functionally usable acoustic hearing throughout the audiometric frequency range in the non-implant ear. First, to establish a baseline, we measured and found slightly impaired pure tone frequency discrimination and nearly perfect melody recognition in all 3 subjects’ acoustic ear. Second, using pure tones in the acoustic ear to match electric pitch induced by an intra-cochlear electrode, we found that the frequency-electrode function was not only 1–2 octaves lower, but also 2 times more compressed in frequency range than the normal cochlear frequency-place function. Third, we derived frequency difference limens in electric pitch and found that the equivalent electric frequency discrimination was 24 times worse than normal-hearing controls. These 3 abnormalities are likely a result of a combination of broad electric field, distant intra-cochlear electrode placement, and non-uniform spiral ganglion cell distribution and survival, all of which are inherent to the electrode-nerve interface in contemporary cochlear implants. Previous studies emphasized on the “mean” shape of the frequency-electrode function, but the present study indicates that the large “variance” of this function, reflecting poor electric pitch discriminability, is the main factor limiting contemporary cochlear implant performance

Auditory Prosthesis with a Penetrating Nerve Array

Contemporary auditory prostheses (“cochlear implants”) employ arrays of stimulating electrodes implanted in the scala tympani of the cochlea. Such arrays have been implanted in some 100,000 profoundly or severely deaf people worldwide and arguably are the most successful of present-day neural prostheses. Nevertheless, most implant users show poor understanding of speech in noisy backgrounds, poor pitch recognition, and poor spatial hearing, even when using bilateral implants. Many of these limitations can be attributed to the remote location of stimulating electrodes relative to excitable cochlear neural elements. That is, a scala tympani electrode array lies within a bony compartment filled with electrically conductive fluid. Moreover, scala tympani arrays typically do not extend to the apical turn of the cochlea in which low frequencies are represented. In the present study, we have tested in an animal model an alternative to the conventional cochlear implant: a multielectrode array implanted directly into the auditory nerve. We monitored the specificity of stimulation of the auditory pathway by recording extracellular unit activity at 32 sites along the tonotopic axis of the inferior colliculus. The results demonstrate the activation of specific auditory nerve populations throughout essentially the entire frequency range that is represented by characteristic frequencies in the inferior colliculus. Compared to conventional scala tympani stimulation, thresholds for neural excitation are as much as 50-fold lower and interference between electrodes stimulated simultaneously is markedly reduced. The results suggest that if an intraneural stimulating array were incorporated into an auditory prosthesis system for humans, it could offer substantial improvement in hearing replacement compared to contemporary cochlear implants