Effects of electrical stimulation in the inferior colliculus on frequency discrimination by rhesus monkeys and implications for the auditory midbrain implant

Daniel S. Pages, Deborah A. Ross, Vanessa M. Puñal, Shruti Agashe, Isaac Dweck, Jerel Mueller, Warren M. Grill, Blake S. Wilson, Jennifer M. Groh

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

Understanding the relationship between the auditory selectivity of neurons and their contribution to perception is critical to the design of effective auditory brain prosthetics. These prosthetics seek to mimic natural activity patterns to achieve desired perceptual outcomes. We measured the contribution of inferior colliculus (IC) sites to perception using combined recording and electrical stimulation. Monkeys performed a frequency-based discrimination task, reporting whether a probe sound was higher or lower in frequency than a reference sound. Stimulation pulses were paired with the probe sound on 50% of trials (0.5- 80µA, 100 -300 Hz, n=172 IC locations in 3 rhesus monkeys). Electrical stimulation tended to bias the animals’ judgments in a fashion that was coarsely but significantly correlated with the best frequency of the stimulation site compared with the reference frequency used in the task. Although there was considerable variability in the effects of stimulation (including impairments in performance and shifts in performance away from the direction predicted based on the site’s response properties), the results indicate that stimulation of the IC can evoke percepts correlated with the frequency-tuning properties of the IC. Consistent with the implications of recent human studies, the main avenue for improvement for the auditory midbrain implant suggested by our findings is to increase the number and spatial extent of electrodes, to increase the size of the region that can be electrically activated, and to provide a greater range of evoked percepts.

Original languageEnglish (US)
Pages (from-to)5071-5083
Number of pages13
JournalJournal of Neuroscience
Volume36
Issue number18
DOIs
StatePublished - May 4 2016

Bibliographical note

Funding Information:
This work was supported in part by the National Institutes of Health (NIH Grant R01EY016478-01 to J.M.G.), the Duke Institute for Brain Sciences (Incubator Award to J.M.G., W.M.G., and Nell Cant), Duke WISeNet (Graduate Fellowship to D.S.P. sponsored by National Science Foundation Grant NSF DGE-1068871). We thank Tom Heil, Jessi Cruger, Karen Waterstradt, Christie Holmes, and the Duke Division of Laboratory Animal Resources for expert technical assistance; Bao Tran-Phu, Aida Ibrahim, Sydney J. Koke, Jessi Cruger, Laura Paulsen, and Diana Friedeberg for assistance with animal training and data collection; and Nell Cant, Deborah Tucci, Kurtis Gruters, and Valeria C. Caruso for insightful commentary and discussion.

Publisher Copyright:
© 2016 the authors.

Keywords

  • Auditory
  • Auditory midbrain implant
  • Electrical stimulation
  • Inferior colliculus
  • Prosthesis

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