The long-term goal of our research is to elucidate neural coding and plasticity mechanisms underlying cortical processing of cochlear implant (CI) signals in the context of vocal communication. We have established a new CI model (the common marmoset) to pursue these questions. The present application builds on that foundation and represents the next key steps towards our long-term objectives. Marmosets have a rich vocal repertoire, are highly communicative, and can potentially be used to study vocal production and auditory feedback mechanisms related to speech processing in CI subjects, which is an area that lacks suitable animal models. The hearing range of the marmoset is similar to that of humans and its auditory cortex shares similar organizations as humans. These similarities make it a highly valuable animal model to address issues in CI research pertaining to human users. The PI's laboratory is a pioneer in marmoset research, and the proposed research will benefit from techniques we developed over the past two decades to study marmoset auditory cortex in awake and behaving conditions.
Aim 1 will compare auditory cortex neuron selectivity for acute and chronic CI stimuli. Our preliminary studies showed that primary auditory cortex (A1) neurons that are acoustically selective to both frequency and sound level are often unresponsive to electrical stimulation of the cochlea. It is not clear how these highly selective cortical neurons behave in the chronic CI stimulation condition.
Aim 2 will define cortical representations of time-varying cochlear implant stimuli in alert primates. Temporally modulated signals are critical components of vocal communication sounds of humans and animals. Previous CI studies in anesthetized animals have encountered limits of cortical phase locking between 20-60 Hz, leaving unanswered the question of how higher frequency envelope modulations, which can be perceived by CI users, are represented in auditory cortex.
Aim 3 will characterize neural responses to CI stimulation in non-primary auditory cortex. Currently, our knowledge on how the auditory cortex processes CI input has almost exclusively relied on studies of A1. Little is known about how cortical areas outside A1 are engaged by CI stimulation at the single neuron level. The results of these aims will help elucidate cortical processes involved in electric hearing and provide insights for improving current cochlear implant designs.

Public Health Relevance

Cochlear implant is the most successful neural prosthetic device. Understanding how the brain processes cochlear electrical stimulation is crucial to the further development of cochlear implant. Findings of the present study will have important implications for understanding speech processing mechanisms in cochlear implant users. Results from this study will help guide new CI technology improvements.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
Research Project (R01)
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Special Emphasis Panel (ZRG1)
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Miller, Roger
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Johns Hopkins University
Biomedical Engineering
Schools of Medicine
United States
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Johnson, Luke A; Della Santina, Charles C; Wang, Xiaoqin (2017) Representations of Time-Varying Cochlear Implant Stimulation in Auditory Cortex of Awake Marmosets (Callithrix jacchus). J Neurosci 37:7008-7022
Johnson, Luke A; Della Santina, Charles C; Wang, Xiaoqin (2016) Selective Neuronal Activation by Cochlear Implant Stimulation in Auditory Cortex of Awake Primate. J Neurosci 36:12468-12484
Wang, Xiaoqin (2016) The Ying and Yang of Auditory Nerve Damage. Neuron 89:680-2
Johnson, Luke A; Della Santina, Charles C; Wang, Xiaoqin (2012) Temporal bone characterization and cochlear implant feasibility in the common marmoset (Callithrix jacchus). Hear Res 290:37-44