NEURONAL RESPONSES IN CAT PRIMARY AUDITORY-CORTEX TO ELECTRICAL COCHLEAR STIMULATION .2. REPETITION RATE CODING

1. Responses of neurons in primary auditory cortex (AI) of the barbitu rate-anesthetized adult cat were studied using cochlear stimulation wi th electrical and acoustic stimuli. Neuronal responses to acoustic sti mulation with brief biphasic clicks of the ear ipsilateral to the stud ied cortical hemisphere were compared with those evoked by electrical stimulation of the contralateral cochlea with brief biphasic electrica l pulses delivered via a feline cochlear prosthesis. The contralateral ear was deafened immediately before implantation of the cochlear pros thesis, The feline cochlear prosthesis consisted of four bipolar elect rode pairs and was placed in the scala tympani. Two bipolar electrode conditions were used for stimulation: one near radial pair with electr ode spacing of 0.25-0.5 mm, and one longitudinal pair with electrode s pacing of similar to 6 mm. 2. The firing rates obtained from single- a nd multiple-neuron recordings were measured as a function of stimulus repetition rate of electrical and acoustic pulses. From period histogr ams over a recording interval of 1,000 ms, the driven firing rate to r epetition rates from 2 to 38 Hz was obtained and repetition rate trans fer functions (RRTFs) were constructed. The RRTFs were characterized a s low-pass or band-pass filters and several descriptors were obtained, such as the repetition rate producing the highest driven activity, hi gh and low cutoff frequencies 6 dB below maximum firing rate, and maxi mum firing rate. 3. For a given neuron, the main characteristics of co rtical RRTFs obtained with electrical and acoustic cochlear stimulatio n were quite similar. However, some small but statistically significan t differences in the best repetition rate, cutoff frequencies, and max imum firing rate could be observed between the different stimulation m odes. The proportion of band-pass RRTFs was larger for electrical stim ulation (57%) than for acoustic stimulation (41%). The high cutoff fre quencies for electrical stimulation were slightly but consistently hig her than for acoustic RRTFs of the same neuron and the maximum firing rate for electrical stimulation was significantly higher than that evo ked by ipsilateral acoustic stimulation. 4. The entrainment of cortica l neurons to electrical and acoustic pulses was determined and entrain ment profiles were constructed. For a given neuron, electrical entrain ment profiles showed higher cutoff frequencies than with acoustic stim ulation when judged with a fixed entrainment criterion of 0.25 spikes per event. The maximum entrainment seen for electrical stimulation was similar to 20% higher than seen for the same neuron with acoustic sti mulation. 5. Correlation analysis of repetition coding and latency par ameters revealed several relationships between these response aspects. Most prominent among them was a significant correlation between measu res of the response latency and estimates of the ability to follow tem poral repetitions for acoustic as well as electrical conditions. 6. Pa rametric and comparative evaluations of cortical responses to acoustic and electrical cochlear stimulation support the conclusion that the t emporal resolution seen in cortical neurons is largely a consequence o f central processing mechanisms based on cell and circuit properties a nd to a lesser degree a consequence of particular spatial and temporal peripheral excitation patterns. The slightly higher temporal resoluti on found for the electrical stimulation modes suggests that the tempor ally highly coherent electrical stimulation appears to engage, in a mo re effective manner, the excitatory/inhibitory mechanisms contributing to the response in Al than acoustic click stimulation with less tempo ral coherence. 7. These results demonstrate that electrical peripheral stimulation is a useful tool for the characterization of physiologica l response properties of auditory neurons and the mechanisms contribut ing to the generation of spectral and temporal receptive field attribu tes, such as the interplay of central inhibitory and excitatory proces ses. In addition, these findings provide important baseline informatio n regarding mechanisms contributing to the creation of perception with electrical stimulation and are crucial for studies of the effects of the chronic use of cochlear prostheses on the functional organization of the auditory cortex.