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The Journal of Neuroscience, October 1, 2008, 28(40):10023-10030; doi:10.1523/JNEUROSCI.1400-08.2008

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Behavioral/Systems/Cognitive
Moment-to-Moment Tracking of State Value in the Amygdala

Marina A. Belova,^1 * Joseph J. Paton,^1 * and C. Daniel Salzman^1,2,3,4,5,6

Departments of ¹Neuroscience and ²Psychiatry, ³W. M. Keck Center on Brain Plasticity and Cognition, ⁴Kavli Institute for Brain Sciences, and ⁵Mahoney Center for Brain and Behavior, Columbia University Medical Center, and ⁶New York State Psychiatric Institute, New York, New York 10032

Correspondence should be addressed to C. Daniel Salzman, Departments of Psychiatry and Neuroscience, 1051 Riverside Drive, Unit 87, Kolb Research Building, New York State Psychiatric Institute, 5-67, New York, NY 10032. Email: cds2005{at}columbia.edu

As an organism interacts with the world, how good or bad things are at the moment, the value of the current state of the organism, is an important parameter that is likely to be encoded in the brain. As the environment changes and new stimuli appear, estimates of state value must be updated to support appropriate responses and learning. Indeed, many models of reinforcement learning posit representations of state value. We examined how the brain mediates this process by recording amygdala neural activity while monkeys performed a trace-conditioning task requiring fixation. The presentation of different stimuli induced state transitions; these stimuli included unconditioned stimuli (USs) (liquid rewards and aversive air puffs), newly learned reinforcement-predictive visual stimuli [conditioned stimuli (CSs)], and familiar stimuli long associated with reinforcement [fixation point (FP)]. The FP had a positive value to monkeys, because they chose to foveate it to initiate trials. Different populations of amygdala neurons tracked the positive or negative value of the current state, regardless of whether state transitions were caused by the FP, CSs, or USs. Positive value-coding neurons increased their firing during the fixation interval and fired more strongly after rewarded CSs and rewards than after punished CSs and air puffs. Negative value-coding neurons did the opposite, decreasing their firing during the fixation interval and firing more strongly after punished CSs and air puffs than after rewarded CSs and rewards. This representation of state value could underlie how the amygdala helps coordinate cognitive, emotional, and behavioral responses depending on the value of one's state.

Key words: amygdala; monkey; state value; reinforcement learning; reward; punishment

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Received April 2, 2008; revised July 30, 2008; accepted Aug. 25, 2008.

Correspondence should be addressed to C. Daniel Salzman, Departments of Psychiatry and Neuroscience, 1051 Riverside Drive, Unit 87, Kolb Research Building, New York State Psychiatric Institute, 5-67, New York, NY 10032. Email: cds2005{at}columbia.edu

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