Auditory experience can reshape cortical maps and transform receptive field properties of neurons in the auditory cortex of the adult animal. The exact form of this plasticity depends on the behavioral context, and the spectrotemporal features of the salient acoustic stimuli. This has been shown by combined physiological and behavioral approaches in our previous experiments in which """"""""on-line"""""""" spectrotemporal receptive fields (STRFs) were rapidly and comprehensively characterized simultaneous with the animal behavior. The experiments also contrasted STRF plasticity in single cells across different auditory tasks employing various acoustic signals with controlled spectral and temporal features. These results are consistent with findings of adaptive plasticity in the motor and other sensory systems and support the hypothesis that auditory cortical cells may undergo rapid, context-dependent changes of their receptive field properties when an animal is engaged in different auditory behavioral tasks. This kind of plasticity would likely involve a selective functional reshaping of the underlying cortical circuitry to sculpt the most effective receptive field for accomplishing the current auditory task. What are the underlying mechanisms that give rise to this extraordinary functional plasticity? The goals of the proposed research are to extend our studies of task-related plasticity to higher order auditory cortical areas, and to a variety of new tasks (including temporal and spectrotemporal tasks), new behavioral paradigms (utilizing either positive or negative reinforcement) and furthermore, to investigate the possible role of top-down signals from frontal cortex in modulating adaptive plasticity in the primary auditory cortex. We propose to rigorously test the hypothesis that frontal cortical neurons encode task rules, expectancies, goals and the task-related meaning of acoustic stimuli, and further, that when an animal performs different auditory tasks, top-down influences from frontal areas contribute to the induction of rapid adaptive plasticity in auditory cortex, that reflects both the nature of the stimuli and goals of the tasks. We shall also combine our physiological experiments with microstimulation in FC and other areas to test if that modulates responses and receptive fields. Our preliminary studies from simultaneous neuronal recordings of single units and local field potentials in auditory and frontal cortex have already lead to exciting new insights, that may lead to progress in understanding the interactions within an extended neuronal network that give rise to adaptive plasticity.

Public Health Relevance

Project Relevance The phenomenon of plasticity that is the focus of the proposed research is fundamental to learning, behavioral performance, and to the repair of the nervous system after damage. Our goal is to understand how plasticity manifests itself in the responses of the auditory cortex, and how do the acoustic stimuli interact with the behavioral feedback to influence the changes in the cortex. The findings of this research could have profound consequences for the design and deployment of hearing aids and cochlear implants.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC005779-09
Application #
8281607
Study Section
Special Emphasis Panel (ZRG1-IFCN-B (02))
Program Officer
Miller, Roger
Project Start
2002-12-01
Project End
2014-06-30
Budget Start
2012-07-01
Budget End
2013-06-30
Support Year
9
Fiscal Year
2012
Total Cost
$301,800
Indirect Cost
$98,157
Name
University of Maryland College Park
Department
Miscellaneous
Type
Schools of Engineering
DUNS #
790934285
City
College Park
State
MD
Country
United States
Zip Code
20742
Ding, Nai; Simon, Jonathan Z; Shamma, Shihab A et al. (2016) Encoding of natural sounds by variance of the cortical local field potential. J Neurophysiol 115:2389-98
Shamma, Shihab A (2015) A convergent tale of two species. Nat Neurosci 18:168-9
Huang, Chengcheng; Englitz, Bernhard; Shamma, Shihab et al. (2015) A neuronal network model for context-dependence of pitch change perception. Front Comput Neurosci 9:101
Sell, Gregory; Suied, Clara; Elhilali, Mounya et al. (2015) Perceptual susceptibility to acoustic manipulations in speaker discrimination. J Acoust Soc Am 137:911-22
Mesgarani, Nima; David, Stephen V; Fritz, Jonathan B et al. (2014) Mechanisms of noise robust representation of speech in primary auditory cortex. Proc Natl Acad Sci U S A 111:6792-7
Shamma, Shihab; Fritz, Jonathan (2014) Adaptive auditory computations. Curr Opin Neurobiol 25:164-8
Atiani, Serin; David, Stephen V; Elgueda, Diego et al. (2014) Emergent selectivity for task-relevant stimuli in higher-order auditory cortex. Neuron 82:486-99
Nelken, Israel; Bizley, Jennifer; Shamma, Shihab A et al. (2014) Auditory cortical processing in real-world listening: the auditory system going real. J Neurosci 34:15135-8
Yin, Pingbo; Fritz, Jonathan B; Shamma, Shihab A (2014) Rapid spectrotemporal plasticity in primary auditory cortex during behavior. J Neurosci 34:4396-408
Laudanski, Jonathan; Torben-Nielsen, Benjamin; Segev, Idan et al. (2014) Spatially distributed dendritic resonance selectively filters synaptic input. PLoS Comput Biol 10:e1003775

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