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The Journal of Neuroscience, April 11, 2007, 27(15):3937-3945; doi:10.1523/JNEUROSCI.5281-06.2007
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Behavioral/Systems/Cognitive
Amygdala Neurons Differentially Encode Motivation and Reinforcement
Kay M. Tye1,2 andPatricia H. Janak1,3 1Ernest Gallo Clinic and Research Center, University of California, San Francisco, Emeryville, California 94608, and 2Graduate Program in Neuroscience and 3Department of Neurology and Wheeler Center for the Neurobiology of Addiction, University of California, San Francisco, San Francisco, California 94143
Correspondence should be addressed to Patricia H. Janak, Ernest Gallo Clinic and Research Center, Department of Neurology, University of California, San Francisco, 5858 Horton Street, Suite 200, Emeryville, CA 94608. Email: pjanak{at}gallo.ucsf.edu
Lesion studies demonstrate that the basolateral amygdala complex (BLA) is important for assigning motivational significance to sensory stimuli, but little is known about how this information is encoded. We used in vivo electrophysiology procedures to investigate how the amygdala encodes motivating and reinforcing properties of cues that induce reinstatement of reward-seeking behavior. Two groups of rats were trained to respond to a sucrose reward. The "paired" group was trained with a reward-predictive cue, whereas the "unpaired" group was trained with a randomly presented cue. Both groups underwent identical extinction and reinstatement procedures during which the reward was withheld. The proportion of neurons that were phasically cue responsive during reinstatement was significantly higher in the paired group (46 of 100) than in the unpaired group (8 of 112). Cues that induce reward-seeking behavior can do so by acting as incentives or reinforcers. Distinct populations of neurons responded to the cue in trials in which the cue acted as an incentive, triggering a motivated reward-seeking state, or as a reinforcer, supporting continued instrumental responding. The incentive motivation-encoding population of neurons (34 of 46 cue-responsive neurons; 74%) extinguished in temporal agreement with a decrease in the rate of instrumental responding. The conditioned reinforcement-encoding population of neurons (12 of 46 cue-responsive neurons; 26%) maintained their response for the duration of cue-reinforced instrumental responding. These data demonstrate that separate populations of cue-responsive neurons in the BLA encode the motivating or reinforcing properties of a cue previously associated with a reward.
Key words: relapse; cue-induced reinstatement; in vivo electrophysiology; addiction; appetitive conditioning; reward
Received Dec. 6, 2006; revised Jan. 29, 2007; accepted Feb. 26, 2007.
Correspondence should be addressed to Patricia H. Janak, Ernest Gallo Clinic and Research Center, Department of Neurology, University of California, San Francisco, 5858 Horton Street, Suite 200, Emeryville, CA 94608. Email: pjanak{at}gallo.ucsf.edu
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