Social contexts are rife with uncertainty. Consequently, much of our sensory apparatus and cognitive skill is applied to reducing this volatility by acquiring information about others. The brain mechanisms that evaluate social information and translate it into decisions, however, remain poorly understood-despite clear dysfunction of these mechanisms in neurological disorders such as autism, social anxiety, and anorexia which are characterized by dysfunctional social motivation and decision making. We hypothesize that social signals are first decoded by several distinct brain areas, including superior temporal sulcus (STS) and amygdala, translated into value signals in the ventral striatum (VS), and transformed into a common currency for comparison and exchange with other types of rewards in the orbital (OFC) and medial prefrontal cortex (mPFC). We propose to use complementary fMRI techniques in human subjects and electrophysiological techniques in macaques to test this hypothesis. Critically, we will use the same psychophysical technique to estimate reward functions for social stimuli in humans and monkeys, thus validating our comparison. Crucially, temporary inactivation of nodes in this network in monkeys and comparison with fMRI results in a high-functioning clinical population with social dysfunction will be used to functionally evaluate our model.

Public Health Relevance

The brain mechanisms that evaluate social information and translate it into decisions remain poorly understood-despite clear dysfunction of these mechanisms in neurological disorders such as autism, social anxiety, and anorexia nervosa which are characterized by dysfunctional social motivation and decision making. We hypothesize that social signals are first decoded by several distinct brain areas, including superior temporal sulcus (STS) and amygdala, translated into value signals in the ventral striatum (VS), and transformed into a common currency for comparison and exchange with other types of rewards in the orbital (OFC) and medial prefrontal cortex (mPFC). We will use complementary fMRI techniques in human subjects and electrophysiological techniques in macaques to test this hypothesis, and functionally validate these observations by determining the locus of dysfunctional social reward processing in a psychiatric population characterized by maladaptive social behavior.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Research Project (R01)
Project #
5R01MH086712-04
Application #
8261124
Study Section
Special Emphasis Panel (ZMH1-ERB-Z (01))
Program Officer
Simmons, Janine M
Project Start
2009-08-01
Project End
2014-02-28
Budget Start
2012-03-01
Budget End
2013-02-28
Support Year
4
Fiscal Year
2012
Total Cost
$585,978
Indirect Cost
$210,351
Name
Duke University
Department
Biology
Type
Schools of Medicine
DUNS #
044387793
City
Durham
State
NC
Country
United States
Zip Code
27705
Roy, Arani; Shepherd, Stephen V; Platt, Michael L (2014) Reversible inactivation of pSTS suppresses social gaze following in the macaque (Macaca mulatta). Soc Cogn Affect Neurosci 9:209-17
Brent, Lauren J N; Chang, Steve W C; Gariepy, Jean-Francois et al. (2014) The neuroethology of friendship. Ann N Y Acad Sci 1316:1-17
Pearson, John M; Watson, Karli K; Platt, Michael L (2014) Decision making: the neuroethological turn. Neuron 82:950-65
Chang, Steve W C; Brent, Lauren J N; Adams, Geoffrey K et al. (2013) Neuroethology of primate social behavior. Proc Natl Acad Sci U S A 110 Suppl 2:10387-94
Carter, R McKell; Huettel, Scott A (2013) A nexus model of the temporal-parietal junction. Trends Cogn Sci 17:328-36
Klein, Jeffrey T; Platt, Michael L (2013) Social information signaling by neurons in primate striatum. Curr Biol 23:691-6
Ebitz, R Becket; Watson, Karli K; Platt, Michael L (2013) Oxytocin blunts social vigilance in the rhesus macaque. Proc Natl Acad Sci U S A 110:11630-5
Chang, Steve W C; Gariepy, Jean-Francois; Platt, Michael L (2013) Neuronal reference frames for social decisions in primate frontal cortex. Nat Neurosci 16:243-50
Heilbronner, Sarah R; Platt, Michael L (2013) Causal evidence of performance monitoring by neurons in posterior cingulate cortex during learning. Neuron 80:1384-91
Pearson, John M; Platt, Michael L (2013) Dopamine: burning the candle at both ends. Neuron 79:831-3

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