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The Journal of Neuroscience, August 25, 2004, 24(34):7557-7565; doi:10.1523/JNEUROSCI.1072-04.2004

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Behavioral/Systems/Cognitive
Repetitive Behaviors in Monkeys Are Linked to Specific Striatal Activation Patterns

Esen Saka,¹ Claudia Goodrich,² Patricia Harlan,³ Bertha K. Madras,² and Ann M. Graybiel³

¹Department of Neurology, Akdeniz University Hospital, 07059 Antalya, Turkey, ²Department of Psychiatry, Harvard Medical School, New England Primate Research Center, Southborough, Massachusetts 01772-9102, and ³Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, and the McGovern Institute for Brain Research, Cambridge, Massachusetts 02139

The spontaneous behavior of humans can be altered dramatically by repeated exposure to psychomotor stimulants. We have developed a primate model for analyzing the neurobiology underlying such drug-induced behavioral changes. We performed ethogram-based behavioral assays on squirrel monkeys given single or multiple cocaine treatments, and in the same monkeys made anatomical plots of striatal neurons that were activated to express early-gene proteins. A final cocaine challenge after chronic intermittent exposure to cocaine induced highly patterned behavioral changes in the monkeys, affecting individual behavioral motifs in distinct ways. In the striatum, the challenge dose induced striosome-predominant expression combined with intense dorsal early-gene expression, especially in the putamen. These patterns of gene expression were highly predictive of the levels of stereotypy exhibited by the monkeys in response to cocaine challenge. The total levels of expression, on the other hand, appeared to reflect increased spontaneous behavioral activation during the drug-free period after the cocaine exposure. We suggest that in the primate, compartmentally and regionally specific striatal activation patterns contribute to the striatal modulation of psychostimulant-induced behaviors. These observations in nonhuman primates raise the possibility that monitoring such basal ganglia activity patterns could help to delineate the neural mechanisms underlying drug-induced repetitive behaviors and related syndromes in which stereotypies are manifest.

Key words: squirrel monkey; behavioral sensitization; cocaine; dopamine; caudate nucleus; putamen; nucleus accumbens; striatum; stereotypy; striosome; matrix

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Received Aug 25, 2003; revised July 14, 2004; accepted July 15, 2004.

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