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The Journal of Neuroscience, September 16, 2009, 29(37):11619-11627; doi:10.1523/JNEUROSCI.3206-09.2009

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Behavioral/Systems/Cognitive
Orbitofrontal and Anterior Cingulate Cortex Neurons Selectively Process Cocaine-Associated Environmental Cues in the Rhesus Monkey

Eun Ha Baeg, Mark E. Jackson, Hank P. Jedema, and Charles W. Bradberry

Departments of Psychiatry and Neuroscience, University of Pittsburgh, Veterans Affairs Pittsburgh Health Services, Pittsburgh, Pennsylvania 15261

Correspondence should be addressed to Charles W. Bradberry, Departments of Psychiatry and Neuroscience, University of Pittsburgh, Veterans Affairs Pittsburgh Health Services, 3501 Fifth Avenue, Room 4078, Pittsburgh, PA 15261. Email: bradberrycw{at}upmc.edu

Encounters with stimuli associated with drug use are believed to contribute to relapse. To probe the neurobiology of environmentally triggered drug use, we have conducted single-unit recordings in rhesus monkeys during presentation of two distinct types of drug paired cues that differentially support drug-seeking. The animals were highly conditioned to these cues via exposure during self-administration procedures conducted over a 4 year period. The cues studied were a discriminative cue that signaled response-contingent availability of cocaine, and a discrete cue that was temporally paired with the cocaine infusion (0.1 or 0.5 mg/kg). Two cortical regions consistently activated by cocaine-associated cues in human imaging studies are the orbitofrontal (OFC) and anterior cingulate cortex (ACC), though little is known about cortical neuronal activity responses to drug cues. We simultaneously recorded single-unit activity in OFC and ACC as well as in dorsal striatum in rhesus monkeys during cocaine self-administration. Dorsal striatal neurons were less engaged by drug cues than cortical regions. Between OFC and ACC, distinct functionality was apparent in neuronal responses. OFC neurons preferentially responded to the discriminative cue, consistent with a role in cue-induced drug-seeking. In contrast, the ACC did not respond more to the discriminative cue than to the discrete cue. Also distinct from the OFC, ACC showed sustained firing throughout the 18 s duration of the discrete cue. This pattern of sustained activation in ACC is consistent with a role in reward expectation and/or in mediating behavioral effects of discrete cues paired with drug infusions.

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Received July 6, 2009; revised Aug. 10, 2009; accepted Aug. 11, 2009.

Correspondence should be addressed to Charles W. Bradberry, Departments of Psychiatry and Neuroscience, University of Pittsburgh, Veterans Affairs Pittsburgh Health Services, 3501 Fifth Avenue, Room 4078, Pittsburgh, PA 15261. Email: bradberrycw{at}upmc.edu

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