The long-term goal of this work is to improve the understanding of neural mechanisms that underlie acoustic communication. This project focuses on the amygdala, a structure known for its role in auditory fear conditioning. For this role, it receives auditory input from the thalamus and cortex, contributes to identifying a stimulu as aversive, and provides for appropriate emotional responses (e.g., autonomic responses, freezing). Recent work demonstrates a broader role for the amygdala in auditory behavior, including acoustic communication. This work is based on the view that the amygdala plays a critical role in acoustic communication through participation in several processes. 1) The amygdala """"""""decides"""""""" whether a vocal signal is salient and whether that salience is positive or negative, based on contextual information from the vocal sequence, other sensory information, and the animal's internal state, 2) It orchestrates emotional responses that are appropriate for the received vocal communication signals and their context, 3) It modulates responsiveness to subsequent vocal signals through its direct and indirect projections to cortical and other auditory structures. In other words, the amygdala is likely to influence how we hear and respond to vocal communication signals. Understanding how the amygdala contributes to acoustic communication has been limited by lack of information on how amygdalar neurons respond to communication signals. Do amygdalar neurons discriminate among social vocalizations? What features of the auditory-evoked spike trains signal discrimination? How does contextual information modify the discrimination and discharge pattern of amygdalar neurons in response to social vocalizations? These questions are addressed within three Specific Aims that investigate the dependence of auditory responses on several forms of stimulus context: acoustic context (the sequencing of composition of vocalizations) (Aims1), other sensory context (Aim 2), and internal state (Aim 3). Auditory responses are obtained using chronic recording from the amygdala of awake, unrestrained animals in most experiments. Two animal models, big brown bats and CBA/CaJ mice, each provide particular advantages for the proposed studies. Dysfunction in the amygdala may play a critical role in abnormal relationships between acoustic inputs and emotional responses in disorders such as autism, schizophrenia, post-traumatic stress, and tinnitus. This work lays groundwork for study of the function of the amygdala in animal models of these disorders.

Public Health Relevance

Dysfunction in the amygdala may play a critical role in the abnormal emotional responses to speech and other sounds that occurs in autism, schizophrenia, post-traumatic stress, and tinnitus. This work will establish how amygdalar neurons normally function in response to speech-like sounds, laying groundwork for study of the function of the amygdala in animal models of these disorders. !

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC000937-23
Application #
8603854
Study Section
Auditory System Study Section (AUD)
Program Officer
Platt, Christopher
Project Start
1990-12-01
Project End
2017-01-31
Budget Start
2014-02-01
Budget End
2015-01-31
Support Year
23
Fiscal Year
2014
Total Cost
$461,475
Indirect Cost
$161,816
Name
Northeast Ohio Medical University
Department
Anatomy/Cell Biology
Type
Schools of Medicine
DUNS #
077779882
City
Rootstown
State
OH
Country
United States
Zip Code
44272
Gadziola, Marie A; Shanbhag, Sharad J; Wenstrup, Jeffrey J (2016) Two distinct representations of social vocalizations in the basolateral amygdala. J Neurophysiol 115:868-86
Grimsley, Jasmine M S; Sheth, Saloni; Vallabh, Neil et al. (2016) Contextual Modulation of Vocal Behavior in Mouse: Newly Identified 12 kHz ""Mid-Frequency"" Vocalization Emitted during Restraint. Front Behav Neurosci 10:38
Grimsley, Calum A; Longenecker, Ryan J; Rosen, Merri J et al. (2015) An improved approach to separating startle data from noise. J Neurosci Methods 253:206-17
Grimsley, Jasmine M S; Hazlett, Emily G; Wenstrup, Jeffrey J (2013) Coding the meaning of sounds: contextual modulation of auditory responses in the basolateral amygdala. J Neurosci 33:17538-48
Wallace, Mark N; Grimsley, Jasmine M S; Anderson, Lucy A et al. (2013) Representation of individual elements of a complex call sequence in primary auditory cortex. Front Syst Neurosci 7:72
Galazyuk, Alexander V; Wenstrup, Jeffrey J; Hamid, Mohamed A (2012) Tinnitus and underlying brain mechanisms. Curr Opin Otolaryngol Head Neck Surg 20:409-15
Wenstrup, Jeffrey James; Nataraj, Kiran; Sanchez, Jason Tait (2012) Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus. Front Neural Circuits 6:75
Grimsley, Jasmine M S; Shanbhag, Sharad J; Palmer, Alan R et al. (2012) Processing of communication calls in Guinea pig auditory cortex. PLoS One 7:e51646
Grimsley, Jasmine M S; Gadziola, Marie A; Wenstrup, Jeffrey J (2012) Automated classification of mouse pup isolation syllables: from cluster analysis to an Excel-based ""mouse pup syllable classification calculator"". Front Behav Neurosci 6:89
Peterson, D C; Wenstrup, J J (2012) Selectivity and persistent firing responses to social vocalizations in the basolateral amygdala. Neuroscience 217:154-71

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