Sound perception is mediated by neural computations in the ventral auditory pathway. This pathway begins in the core auditory cortex-specifically, the primary auditory cortex and the rostral field R. These core areas project to the anterolateral (AL) and middle-lateral belt regions of the auditory cortex. In turn, these belt regions project directly and indirectly to the ventrolateral prefrontal cortex (vPFC). Although there is broad agreement that this pathway is critical for sound perception, there is no consensus on the contribution of different regions of this pathway to sound perception. This grant proposal closes this knowledge gap by identifying how sound perception arises from neural activity and the hierarchical flow of information processing in the ventral auditory pathway. Thus, the overarching goal of this grant proposal is to identify the systems-level properties of the brain that contribute to sound perception.
In Aim #1, we identify the hierarchica flow of information processing in the ventral pathway that underlies a listener's ability to segregate and group auditory stimuli into one or more sounds. To address this gap in our knowledge, neural activity is recorded while monkeys participate in an """"""""auditory-streaming"""""""" task. This one-interval, two-alternative forced-choice task requires the monkey to report whether they hear one or two auditory streams. The auditory stimulus is a sequence of tone bursts. On a trial- by-trial basis, we systematically manipulate the properties of the sequence, which changes the probability that the monkey reports one or two auditory streams. While the monkeys are participating in this task, spiking activity is recorded in core auditory cortex, AL, and vPFC. The data generated from this task test the hypotheses that (1) neural activity in core auditory cortex is modulated by the spectral and temporal properties of the auditory stimulus, but this modulation correlates poorly with the monkey's behavior;(2) neural activity in AL is better correlated with behavioral performance;and (3) vPFC activity correlates best with the monkey's behavior.
In Aim #2, we identify the neural-population codes in the ventral pathway underlying a listener's tolerance to identity-preserving changes in a sound. To address this knowledge gap, we record neural activity while monkeys listen and attend to different sounds and identity-preserving transformations of these sounds. We hypothesize that, in the ventral pathway, neural-population codes underlying a listener's tolerance to identity-preserving changes in a sound are first found in AL. More specifically, we hypothesize that (1) AL spiking activity is more invariant to identity-preserving changes in a sound than activity in core auditory cortex;(2) average sparseness is the same in core auditory cortex and AL;and (3) on a neuron-by-neuron basis, sparseness is positively correlated with local-feature sensitivity but inversely correlated with single-neuron tolerance.

Public Health Relevance

The results of this grant proposal will reveal strategies used by the brain to form representations of sounds. These findings may provide a fuller understanding of hearing, hearing loss, and mental-health issues such as attention-deficit syndrome and schizophrenia associated with dysfunctions in attention. The insights from these studies will also improve the design of hearing prosthetics, diagnostic assays, and the development of rehabilitation programs.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
Research Project (R01)
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Special Emphasis Panel (SPC)
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Platt, Christopher
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University of Pennsylvania
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Cohen, Yale E; Bennur, Sharath; Christison-Lagay, Kate et al. (2016) Functional Organization of the Ventral Auditory Pathway. Adv Exp Med Biol 894:381-388
Johnston, Jessica M; Cohen, Yale E; Shirley, Harry et al. (2016) Recent refinements to cranial implants for rhesus macaques (Macaca mulatta). Lab Anim (NY) 45:180-6
Tsunada, Joji; Liu, Andrew S K; Gold, Joshua I et al. (2016) Causal contribution of primate auditory cortex to auditory perceptual decision-making. Nat Neurosci 19:135-42
Liu, Andrew S K; Tsunada, Joji; Gold, Joshua I et al. (2015) Temporal Integration of Auditory Information Is Invariant to Temporal Grouping Cues eNeuro 2:
Christison-Lagay, Kate L; Gifford, Adam M; Cohen, Yale E (2015) Neural correlates of auditory scene analysis and perception. Int J Psychophysiol 95:238-245
Christison-Lagay, Kate L; Bennur, Sharath; Blackwell, Jennifer et al. (2014) Natural variability in species-specific vocalizations constrains behavior and neural activity. Hear Res 312:128-42
Gifford, Adam M; Cohen, Yale E; Stocker, Alan A (2014) Characterizing the impact of category uncertainty on human auditory categorization behavior. PLoS Comput Biol 10:e1003715
Bizley, Jennifer K; Cohen, Yale E (2013) The what, where and how of auditory-object perception. Nat Rev Neurosci 14:693-707
Habbershon, Holly M; Ahmed, Sarah Z; Cohen, Yale E (2013) Rhesus macaques recognize unique multimodal face-voice relations of familiar individuals and not of unfamiliar ones. Brain Behav Evol 81:219-25
Bennur, Sharath; Tsunada, Joji; Cohen, Yale E et al. (2013) Understanding the neurophysiological basis of auditory abilities for social communication: a perspective on the value of ethological paradigms. Hear Res 305:3-9

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