Selective Neuronal Activation by Cochlear Implant Stimulation in Auditory Cortex of Awake Primate

Abstract

Despite the success of cochlear implants (CIs) in human populations, most users perform poorly in noisy environments and music and tonal language perception. How CI devices engage the brain at the single neuron level has remained largely unknown, in particular in the primate brain. By comparing neuronal responses with acoustic and CI stimulation in marmoset monkeys unilaterally implanted with a CI electrode array, we discovered that CI stimulation was surprisingly ineffective at activating many neurons in auditory cortex, particularly in the hemisphere ipsilateral to the CI. Further analyses revealed that the CI-nonresponsive neurons were narrowly tuned to frequency and sound level when probed with acoustic stimuli; such neurons likely play a role in perceptual behaviors requiring fine frequency and level discrimination, tasks that CI users find especially challenging. These findings suggest potential deficits in central auditory processing of CI stimulation and provide important insights into factors responsible for poor CI user performance in a wide range of perceptual tasks.

Optogenetic stimulation of cochlear neurons activates the auditory pathway and restores auditory-driven behavior in deaf adult gerbils

“…Recordings of singleneuron firing in AI confirmed this energy threshold. A recent study in awake primates demonstrated that about 40% of neurons in the auditory cortex could be driven by contralateral eCI stimulation (27), whereas we observed 52% of neurons driven by oCI in the gerbil.…”

Tracking Down Nonresponsive Cortical Neurons in Cochlear Implant Stimulation

“…Taken together, these data suggest that the marmoset AC in the study by Johnson et al (2016) has a history of experience with real sounds but not the kind of stimulation produced by CIs. Future experiments using the CI marmoset model could test the hypothesis that O-units are important for CI performance in noisy surroundings.…”

Representations of Time-Varying Cochlear Implant Stimulation in Auditory Cortex of Awake Marmosets (Callithrix jacchus)

“…Each neuron was tested for both acoustic and CI responsiveness with a range of repetition or stimulation rates and sound or current levels (see Materials and Methods). Note that a neuron could be responsive to both acoustic and CI stimulation or only one modality (Johnson et al, 2016). After finding a CI stimulus that evoked firing in the neuron, an electrode-tuning function (Figs.…”

“…Of these, 187 were responsive to CI pulse trains and 237 were responsive to acoustic click trains. Our recent work showed that the left hemisphere (contralateral to CI) was much more responsive to CI than the right hemisphere (Johnson et al, 2016). Therefore, the population data of CI-responsive units consisted of 159 units from left hemispheres and 28 units from right hemispheres.…”