Effects of Electrical Stimulation in the Inferior Colliculus on Frequency Discrimination by Rhesus Monkeys and Implications for the Auditory Midbrain Implant.

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 (0.5-80 μA, 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.Patients with hearing loss stemming from causes that interrupt the auditory pathway after the cochlea need a brain prosthetic to restore hearing. Recently, prosthetic stimulation in the human inferior colliculus (IC) was evaluated in a clinical trial. Thus far, speech understanding was limited for the subjects and this limitation is thought to be partly due to challenges in harnessing the sound frequency representation in the IC. Here, we tested the effects of IC stimulation in monkeys trained to report the sound frequencies they heard. Our results indicate that the IC can be used to introduce a range of frequency percepts and suggest that placement of a greater number of electrode contacts may improve the effectiveness of such implants.

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Citation

Published Version (Please cite this version)

10.1523/JNEUROSCI.3540-15.2016

Publication Info

Pages, Daniel S, Deborah A Ross, Vanessa M Puñal, Shruti Agashe, Isaac Dweck, Jerel Mueller, Warren M Grill, Blake S Wilson, et al. (2016). Effects of Electrical Stimulation in the Inferior Colliculus on Frequency Discrimination by Rhesus Monkeys and Implications for the Auditory Midbrain Implant. The Journal of neuroscience : the official journal of the Society for Neuroscience, 36(18). pp. 5071–5083. 10.1523/JNEUROSCI.3540-15.2016 Retrieved from https://hdl.handle.net/10161/17889.

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Scholars@Duke

Agashe

Shruti Agashe

Assistant Professor of Neurology

My patients have motivated me to be involved in clinical research. My interests spans areas such as identification of biomarkers in epilepsy, pre-surgical evaluation in epilepsy including stereoEEG as well as drugs and device trials. Given my training in biomedical engineering, I have a special interest in Neuromodulation including deep brain stimulation, responsive neurostimulation, minimally invasive device therapies as well as developing novel neuromodulation techniques for use in epilepsy care.

Grill

Warren M. Grill

Edmund T. Pratt, Jr. School Distinguished Professor of Biomedical Engineering

Our research employs engineering approaches to understand and control neural function. We work on fundamental questions and applied development in electrical stimulation of the nervous system to restore function to individuals with neurological impairment or injury.

Current projects include:
• understanding the mechanisms of and developing advanced approaches to deep brain stimulation to treat movement disorders,
• developing novel approaches to peripheral nerve electrical stimulation for restoration of bladder function, 
• understanding the mechanisms of and developing advanced approaches to spinal cord stimulation to treat chronic pain,
• understanding and controlling the cellular effects of transcranial magnetic stimulation, and
• design of novel electrodes and waveforms for selective stimulation of the nervous system.

Wilson

Blake Shaw Wilson

Adjunct Professor in the Department of Head and Neck Surgery & Communication Sciences

Prof. Wilson is the Director of the Duke Hearing Center and is an Adjunct or Consulting Professor in each of three departments at Duke: Head and Neck Surgery & Communication Sciences, Biomedical Engineering, and Electrical and Computer Engineering. He has been involved in the development of the cochlear implant (CI) for four decades and is the inventor of many of the signal processing strategies used with the present-day CIs. One of his papers, in the journal Nature, is the most highly cited publication in the principal field of CIs. He also has become keenly interested in global hearing healthcare and presently is the Chair of the Lancet Commission on Hearing Loss. He or he and his teams or colleagues have been recognized with a high number of awards and honors, including the 2015 Russ Prize, “for engineering cochlear implants that allow the deaf to hear,” and the 2013 Lasker~DeBakey Award, “for the development of the modern cochlear implant – a device that bestows hearing to individuals with profound deafness.” The Russ Prize is the world’s top honor for bioengineering and the Lasker Awards are second only to the Nobel Prize in Physiology or Medicine for recognizing advances in medicine and medical science. Prof. Wilson is a recipient of the Distinguished Alumni Award from the Pratt School of Engineering at Duke (in 2007) and from the University as a whole (in 2019; the 42nd recipient of that Award). Additionally, he is a member of the USA’s National Academy of Engineering and is a Fellow of the Institute of Electrical and Electronics Engineers, the Acoustical Society of America, and the National Academy of Inventors.

Groh

Jennifer M. Groh

Professor of Psychology and Neuroscience

Research in my laboratory concerns how sensory and motor systems work together, and how neural representations play a combined role in sensorimotor and cognitive processing (embodied cognition).

Most of our work concerns the interactions between vision and hearing. We frequently perceive visual and auditory stimuli as being bound together if they seem likely to have arisen from a common source. That's why we tend not to notice that the speakers on TV sets or in movie theatres are located beside, and not behind, the screen. Research in my laboratory is devoted to investigating the question of how the brain coordinates the information arising from the ears and eyes. Our findings challenge the historical view of the brain's sensory processing as being automatic, autonomous, and immune from outside influence. We have recently established that neurons in the auditory pathway (inferior colliculus, auditory cortex) alter their responses to sound depending on where the eyes are pointing. This finding suggests that the different sensory pathways meddle in one another's supposedly private affairs, making their respective influences felt even at very early stages of processing. The process of bringing the signals from two different sensory pathways into a common frame of reference begins at a surprisingly early point along the primary sensory pathways.


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