Electrical cochlear stimulation in the deaf cat: comparisons between psychophysical and central auditory neuronal thresholds.

Cochlear prostheses for electrical stimulation of the auditory nerve ("electrical hearing") can provide auditory capacity for profoundly deaf adults and children, including in many cases a restored ability to perceive speech without visual cues. A fundamental challenge in auditory neuroscience is to understand the neural and perceptual mechanisms that make rehabilitation of hearing possible in these deaf humans. We have developed a feline behavioral model that allows us to study behavioral and physiological variables in the same deaf animals. Cats deafened by injection of ototoxic antibiotics were implanted with either a monopolar round window electrode or a multichannel scala tympani electrode array. To evaluate the effects of perceptually significant electrical stimulation of the auditory nerve on the central auditory system, an animal was trained to avoid a mild electrocutaneous shock when biphasic current pulses (0.2 ms/phase) were delivered to its implanted cochlea. Psychophysical detection thresholds and electrical auditory brain stem response (EABR) thresholds were estimated in each cat. At the conclusion of behavioral testing, acute physiological experiments were conducted, and threshold responses were recorded for single neurons and multineuronal clusters in the central nucleus of the inferior colliculus (ICC) and the primary auditory cortex (A1). Behavioral and neurophysiological thresholds were evaluated with reference to cochlear histopathology in the same deaf cats. The results of the present study include: 1) in the cats implanted with a scala tympani electrode array, the lowest ICC and A1 neural thresholds were virtually identical to the behavioral thresholds for intracochlear bipolar stimulation; 2) behavioral thresholds were lower than ICC and A1 neural thresholds in each of the cats implanted with a monopolar round window electrode; 3) EABR thresholds were higher than behavioral thresholds in all of the cats (mean difference = 6.5 dB); and 4) the cumulative number of action potentials for a sample of ICC neurons increased monotonically as a function of the amplitude and the number of stimulating biphasic pulses. This physiological result suggests that the output from the ICC may be integrated spatially across neurons and temporally integrated across pulses when the auditory nerve array is stimulated with a train of biphasic current pulses. Because behavioral thresholds were lower and reaction times were faster at a pulse rate of 30 pps compared with a pulse rate of 2 pps, spatial-temporal integration in the central auditory system was presumably reflected in psychophysical performance.

Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. III. Activation patterns in short- and long-term deafness.

The effects of auditory deprivation on the spatial distribution of cortical response thresholds to electrical stimulation of the adult cat cochlea were evaluated. Threshold distributions for single- and multiple-unit responses from the middle cortical layers were obtained on the ectosylvian gyrus in three groups of animals: adult, acutely implanted animals ("acute group"); adult animals, 2 wk after deafening and implantation ("short-term group"); adult, neonatally deafened animals ("long-term group") implanted after 2-5 years of deafness. For all three groups, we observed similar patterns of circumscribed regions of low response thresholds in the region of primary auditory cortex (AI). A dorsal and a ventral region of low response thresholds were found separated by a narrow, anterior-posterior strip of elevated thresholds. The two low-threshold regions in the acute and the short-term group were arranged cochleotopically. This was reflected in a systematic shift of the cortical locations with minimum thresholds as a function of cochlear position of the radial and monopolar stimulation electrodes. By contrast, the long-term deafened animals maintained only weak or no signs of cochleotopicity. In some cases of this group, significant deviations from a simple tri-partition of the dorsoventral axis of AI was observed. Analysis of the spatial extent of the low-threshold regions revealed that the activated area in acute cases was significantly smaller than the long- and the short-term cases for both dorsal and ventral AI. There were no significant differences in the rostrocaudal extent of activation between long- and short-term deafening, although the total activated area in the short-term cases was larger than in long-term deafened animals. The width of the narrow high-threshold ridge that separated the dorsal and ventral low-threshold regions was the widest for the acute cases and the narrowest for the short-term deafened animals. The findings of relative large differences in cortical response distributions between the acute and short-term animals suggests that the effects observed in long-term deafened animals are not solely a consequence of loss of peripheral innervation density. The effects may reflect electrode-specific effects or reorganizational changes based on factors such as differences in excitatory and inhibitory balance.

Temporal processing in cat primary auditory cortex.

In this short review, we discuss several aspects of how temporal coding is reflected in the response of primary auditory cortical neurons. We attempt to establish a link between several different temporal response properties including onset latency, response strength to repetitive stimuli, and the recovery of a response from suppression by a preceding signal. The results suggest a relationship between temporal effects that are expressed at quite different time scales. The results are discussed in relation to spatial representational properties and to coding in other sensory cortices.

Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. II. Repetition rate coding.

1. Responses of neurons in primary auditory cortex (AI) of the barbiturate-anesthetized adult cat were studied using cochlear stimulation with electrical and acoustic stimuli. Neuronal responses to acoustic stimulation with brief biphasic clicks of the ear ipsilateral to the studied cortical hemisphere were compared with those evoked by electrical stimulation of the contralateral cochlea with brief biphasic electrical pulses delivered via a feline cochlear prosthesis. The contralateral ear was deafened immediately before implantation of the cochlear prosthesis. The feline cochlear prosthesis consisted of four bipolar electrode pairs and was placed in the scala tympani. Two bipolar electrode conditions were used for stimulation: one near radial pair with electrode spacing of 0.25-0.5 mm, and one longitudinal pair with electrode spacing of approximately 6 mm. 2. The firing rates obtained from single- and multiple-neuron recordings were measured as a function of stimulus repetition rate of electrical and acoustic pulses. From period histograms over a recording interval of 1,000 ms, the driven firing rate to repetition rates from 2 to 38 Hz was obtained and repetition rate transfer functions (RRTFs) were constructed. The RRTFs were characterized as low-pass or band-pass filters and several descriptors were obtained, such as the repetition rate producing the highest driven activity, high and low cutoff frequencies 6 dB below maximum firing rate, and maximum firing rate. 3. For a given neuron, the main characteristics of cortical RRTFs obtained with electrical and acoustic cochlear stimulation were quite similar. However, some small but statistically significant differences in the best repetition rate, cutoff frequencies, and maximum firing rate could be observed between the different stimulation modes. The proportion of band-pass RRTFs was larger for electrical stimulation (57%) than for acoustic stimulation (41%). The high cutoff frequencies for electrical stimulation were slightly but consistently higher than for acoustic RRTFs of the same neuron and the maximum firing rate for electrical stimulation was significantly higher than that evoked by ipsilateral acoustic stimulation. 4. The entrainment of cortical neurons to electrical and acoustic pulses was determined and entrainment profiles were constructed. For a given neuron, electrical entrainment profiles showed higher cutoff frequencies than with acoustic stimulation when judged with a fixed entrainment criterion of 0.25 spikes per event. The maximum entrainment seen for electrical stimulation was approximately 20% higher than seen for the same neuron with acoustic stimulation. 5. Correlation analysis of repetition coding and latency parameters revealed several relationships between these response aspects. Most prominent among them was a significant correlation between measures of the response latency and estimates of the ability to follow temporal repetitions for acoustic as well as electrical conditions. 6. Parametric and comparative evaluations of cortical responses to acoustic and electrical cochlear stimulation support the conclusion that the temporal resolution seen in cortical neurons is largely a consequence of central processing mechanisms based on cell and circuit properties and to a lesser degree a consequence of particular spatial and temporal peripheral excitation patterns. The slightly higher temporal resolution found for the electrical stimulation modes suggests that the temporally highly coherent electrical stimulation appears to engage, in a more effective manner, the excitatory/inhibitory mechanisms contributing to the response in AI than acoustic click stimulation with less temporal coherence. (ABSTRACT TRUNCATED)

Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. I. Intensity dependence of firing rate and response latency.

1. Responses of neurons in primary auditory cortex (AI) of the barbiturate anesthetized adult cat were studied using cochlear stimulation with electrical and acoustic stimuli. Acoustic stimulation of the ear ipsilateral to the studied cortical hemisphere with brief biphasic clicks was compared with electrical stimulation of the contralateral cochlea with brief biphasic electrical pulses delivered via a feline cochlear prosthesis. The contralateral ear was deafened immediately before implantation of the cochlear prosthesis. The feline cochlear prosthesis consisted of four bipolar electrode pairs and was placed in the scala tympani. Two bipolar electrode conditions were used for stimulation: one near radial pair with electrode spacing of approximately 0.5 mm, and one longitudinal pair with electrode spacing of approximately 6 mm. 2. The firing rates obtained from single- and multiple-neuron recordings were measured as a function of stimulus intensity for single electrical and acoustic pulses. Resulting rate/level functions were characterized by a fast growing low-level segment and a more slowly growing, saturating, or decreasing high-level segment. The slopes of these two segments as well as the stimulus level and firing rate at the juncture of these two segments (the transition point) provide a complete characterization of the response magnitude behavior as a function of stimulus intensity. 3. The main characteristics of rate/level functions obtained with electrical and acoustic cochlear stimulation were quite similar. However, for any given neuron, differences in the primary growth behavior, such as monotonic or nonmonotonic growth, could be observed between the different stimulation modes. 4. Response latencies from single- and multiple-neuron recordings were obtained as a function of stimulus intensity for electrical and acoustic pulses. Resulting latency/level functions were characterized by a rapidly decreasing low-level segment and a more slowly decreasing high-level segment. The slopes of these two segments as well as the stimulus level and response latency at the juncture of these two segments (the transition point) provide a complete characterization of the response latency behavior as a function of stimulus intensity. Transition point levels for the rate/level function and the latency/level were nearly identical. 5. The characteristic latency behavior for each neuronal response was found to be very similar for acoustic and electrical stimulation. Correlation analysis revealed a close relationship between latency parameters of the two electrical stimulation conditions, a weaker relationship between the longitudinal electrical and the acoustic conditions, and the weakest relationship between the radial electrical and acoustic conditions. 6. Correlation analysis for rate and latency parameters revealed several relationships between these response aspects.(ABSTRACT TRUNCATED AT 400 WORDS)

Analysis and revision of the minimal auditory capabilities (MAC) battery.

The Minimal Auditory Capabilities (MAC) Battery was administered individually to 75 hearing aid users with profound sensorineural hearing loss. The purposes of the study were (1) to determine the reliability of the individual tests, their range of difficulty, and their intercorrelations; (2) to undertake a standardization procedure based on data from this population; and (3) to assess the need for revisions. Difficulty ranged gradually from a mean score of 86% correct for the Spondee Same/Different test to a mean of 16% for the NU 6 monosyllabic word test. Alpha estimates of reliability were 0.89 or higher for all but the Everyday Sounds test (0.85), the Question/Statement test (0.83), and the Spondee Same/Different test (0.81). Along with the reliability and range of difficulty results, interest correlations provided no indication that any of the tests should be discarded. In the standardization of the MAC, the mean score correct on each test was set at 100 and the standard deviation at 10. Prepared tables for immediate conversion of a raw score to a standardized score for any test are included in an Appendix. Among revisions, also listed in the Appendix, the CID Everyday Sentences test was reduced to 20 items from 40, the SPIN High-Context Sentences were assigned key words, and the assessment of distinctive feature identification was discontinued.