Vocal communication is important for human learning and social interaction. Speech perception impairments are features of neurological disorders such as auditory processing disorder (APD) and autism. In APD patients and some learning-disabled children, abnormalities in the neural processing of spectrotemporally complex sounds such as those in vocalizations are observed. The goal of this research is to understand how auditory learning (perception) and vocal learning (production) affect the neural processing of vocalizations and other sounds. Animals that learn to recognize and produce complex communication vocalizations are appropriate model systems in which to study how learning alters the neural coding of vocalizations. Songbirds are well suited for this research because: 1) they are highly skilled in auditory recognition learning;2) they learn to produce their own vocalizations by vocal imitation, like humans but unlike most other animals;and 3) the auditory brain regions that process vocalizations are known. Songbirds also produce different behavioral responses to vocalizations that differ in behavioral importance, or salience. In our model species, the zebra finch, auditory midbrain neurons produce robust and reliable responses to a wide range of sounds, including complex vocalizations. Studies will test three main hypotheses. First, auditory recognition learning alters the midbrain encoding of songs and other sounds (Aim 1). We will train adult birds to recognize and respond to specific songs and then compare the responses of midbrain neurons to recognizable songs and untrained songs. Predicted differences in the neural responses to recognizable and untrained songs are spike rate, neural discrimination, spectral tuning and spectrotemporal tuning. Second, the responses of midbrain neurons to vocalizations depend on the behavioral salience of vocalizations (Aim 2). We will train adult birds to associate positive or negative behavioral salience with specific songs, and then compare the responses of midbrain neurons to salient songs with positive and negative valence, and songs without trained salience. Third, song learning (learning to produce songs by imitation) alters midbrain encoding of songs (Aim 3). We will raise juvenile birds under conditions in which song learning does and does not occur, and compare the auditory responses of midbrain neurons from birds that have and have not learned to produce song. The proposed experiments will use behavioral training/testing, neurophysiology, computational data analysis, anatomical analysis, and manipulations in vocal learning to identify how learning shapes neuronal responses to communication vocalizations. Understanding the effects of auditory and vocal learning on sound coding in vocal learners may provide candidate neural mechanisms for how auditory training alters speech coding in the human brain and ideas about how speech acquisition shapes speech processing.

Public Health Relevance

Deficits in vocal communication are hallmarks of human disorders such as auditory processing disorder (APD) and autism, and interfere with learning, social interactions and work productivity. The proposed research will test the effects of adult auditory learning and juvenile vocal learning on neuronal responses to vocalizations and other sounds in the auditory midbrain. The neural mechanisms of vocal perception that are described in this work may suggest candidate mechanisms for how auditory training alters human brain processing of speech sounds and how speech acquisition shapes speech processing.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC009810-03
Application #
8225299
Study Section
Auditory System Study Section (AUD)
Program Officer
Platt, Christopher
Project Start
2010-03-01
Project End
2015-02-28
Budget Start
2012-03-01
Budget End
2013-02-28
Support Year
3
Fiscal Year
2012
Total Cost
$383,077
Indirect Cost
$141,077
Name
Columbia University (N.Y.)
Department
Psychology
Type
Other Domestic Higher Education
DUNS #
049179401
City
New York
State
NY
Country
United States
Zip Code
10027
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Calabrese, Ana; Woolley, Sarah M N (2015) Coding principles of the canonical cortical microcircuit in the avian brain. Proc Natl Acad Sci U S A 112:3517-22
Schneider, David M; Woolley, Sarah M N (2013) Sparse and background-invariant coding of vocalizations in auditory scenes. Neuron 79:141-52
Woolley, Sarah M N; Portfors, Christine V (2013) Conserved mechanisms of vocalization coding in mammalian and songbird auditory midbrain. Hear Res 305:45-56
Woolley, Sarah M N (2012) Early experience shapes vocal neural coding and perception in songbirds. Dev Psychobiol 54:612-31
Schumacher, Joseph W; Schneider, David M; Woolley, Sarah M N (2011) Anesthetic state modulates excitability but not spectral tuning or neural discrimination in single auditory midbrain neurons. J Neurophysiol 106:500-14
Ramirez, Alexandro D; Ahmadian, Yashar; Schumacher, Joseph et al. (2011) Incorporating naturalistic correlation structure improves spectrogram reconstruction from neuronal activity in the songbird auditory midbrain. J Neurosci 31:3828-42
Woolley, Sarah M N; Moore, Jordan M (2011) Coevolution in communication senders and receivers: vocal behavior and auditory processing in multiple songbird species. Ann N Y Acad Sci 1225:155-65
Calabrese, Ana; Schumacher, Joseph W; Schneider, David M et al. (2011) A generalized linear model for estimating spectrotemporal receptive fields from responses to natural sounds. PLoS One 6:e16104
Sanes, Dan H; Woolley, Sarah M N (2011) A behavioral framework to guide research on central auditory development and plasticity. Neuron 72:912-29

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