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The Journal of Neuroscience, September 9, 2009, 29(36):11215-11225; doi:10.1523/JNEUROSCI.6096-08.2009

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Behavioral/Systems/Cognitive
Orexin A/Hypocretin-1 Selectively Promotes Motivation for Positive Reinforcers

Stephanie L. Borgland,1,5 Shao-Ju Chang,1 M. Scott Bowers,1 Jennifer L. Thompson,5 Nicole Vittoz,3 Stan B. Floresco,4 Jonathan Chou,1 Billy T. Chen,1 and Antonello Bonci1,2

1Ernest Gallo Clinic and Research Center, Department of Neurology, and 2Wheeler Center for the Neurobiology of Addiction, University of California, San Francisco, San Francisco, California 94110, 3Department of Psychiatry, The University of British Columbia, Vancouver, British Columbia V6T 2B5, Canada, and Departments of 4Psychology and 5Anesthesiology, Pharmacology, and Therapeutics, The University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada

Correspondence should be addressed to Stephanie L. Borgland, Department of Anesthesiology, Pharmacology, and Therapeutics, The University of British Columbia, 212-2176 Health Sciences Mall, Vancouver, BC V6T 1Z3, Canada. Email: Borgland{at}interchange.ubc.ca

Orexin A/hypocretin-1 (oxA/hcrt-1) is known to be a modulator of dopamine-dependent neuronal activity and behaviors. However, the role of this system in driving motivated behaviors remains poorly understood. Here, we show that orexin/hypocretin receptor-1 (ox/hcrt-1R) signaling is important for motivation for highly salient, positive reinforcement. Blockade of ox/hcrt-1R selectively reduced work to self-administer cocaine or high fat food pellets. Moreover, oxA/hcrt-1 strengthened presynaptic glutamatergic inputs to the ventral tegmental area (VTA) only in cocaine or high fat self-administering rats. Finally, oxA/hcrt-1-mediated excitatory synaptic transmission onto VTA neurons was not potentiated following an arousing, aversive stimulus, suggesting that oxA/hcrt-1-mediated glutamatergic synaptic transmission was potentiated selectively with highly salient positive reinforcers. These experiments provide evidence for a selective role of oxA/hcrt-1 signaling in motivation for highly salient reinforcers and may represent a unique opportunity to design novel therapies that selectively reduce excessive drive to consume positive reinforcers of high salience.

Received Dec. 19, 2008; revised July 28, 2009; accepted July 31, 2009.

Correspondence should be addressed to Stephanie L. Borgland, Department of Anesthesiology, Pharmacology, and Therapeutics, The University of British Columbia, 212-2176 Health Sciences Mall, Vancouver, BC V6T 1Z3, Canada. Email: Borgland{at}interchange.ubc.ca
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