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

Cochlear prostheses for electrical stimulation of the auditory nerve ("elec trical hearing") can provide auditory capacity for profoundly deaf adults a nd 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 o f hearing possible in these deaf humans. We have developed a feline behavio ral 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 multicha nnel scala tympani electrode array. To evaluate the effects of perceptually significant electrical stimulation of the auditory nerve on the central au ditory system, an animal was trained to avoid a mild electrocutaneous shock when biphasic current pulses (0.2 ms/phase) were delivered to its implante d cochlea. Psychophysical detection thresholds and electrical auditory brai n stem response (EABR) thresholds were estimated in each cat. At the conclu sion 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 p rimary auditory cortex (A1). Behavioral and neurophysiological thresholds w ere evaluated with reference to cochlear histopathology in the same deaf ca ts. 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 w ere virtually identical to the behavioral thresholds for intracochlear bipo lar stimulation; 2) behavioral thresholds were lower than ICC and A1 neural thresholds in each of the cats implanted with a monopolar round window ele ctrode; 3) EABR thresholds were higher than behavioral thresholds in all of the cats (mean difference = 6.5 dB); and 4) the cumulative number of actio n potentials for a sample of ICC neurons increased monotonically as a funct ion of the amplitude and the number of stimulating biphasic pulses. This ph ysiological result suggests that the output from the ICC may he integrated spatially across neurons and temporally integrated across pulses when the a uditory 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-tempora l integration in the central auditory system was presumably reflected in ps ychophysical performance.