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The Journal of Neuroscience, October 10, 2007, 27(41):11075-11082; doi:10.1523/JNEUROSCI.3542-07.2007

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Behavioral/Systems/Cognitive
Orexin Signaling in the Ventral Tegmental Area Is Required for High-Fat Appetite Induced by Opioid Stimulation of the Nucleus Accumbens

Huiyuan Zheng, Laurel M. Patterson, and Hans-Rudolf Berthoud

Neurobiology of Nutrition Laboratory, Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana 70808

Correspondence should be addressed to Hans-Rudolf Berthoud, Pennington Biomedical Research Center, 6400 Perkins Road, Baton Rouge, LA 70808. Email: berthohr{at}pbrc.edu

The overriding of satiety and homeostatic control mechanisms by cognitive, rewarding, and emotional aspects of palatable foods may contribute to the evolving obesity crisis, but little is known about neural pathways and mechanisms responsible for crosstalk between the "cognitive" and "metabolic" brain in the control of appetite. Here we show that neural connections between the nucleus accumbens and hypothalamus might be part of this link. Using the well known model of selective stimulation of high-fat intake induced by intra-accumbens injection of the µ-opioid receptor agonist D-Ala2-N-Me-Phe⁴-gly⁵-ol-enkephalin (DAMGO), we demonstrate that orexin signaling in the ventral tegmental area is important for this reward-driven appetite to override metabolic repletion signals in presatiated rats. We further show that accumbens DAMGO in the absence of food selectively increases the proportion of orexin neurons expressing c-Fos in parts of the perifornical hypothalamus and that neural projections originating in DAMGO-responsive sites of the nucleus accumbens make close anatomical contacts with hypothalamic orexin neurons. These findings suggest that direct accumbens–hypothalamic projections can stimulate hypothalamic orexin neurons, which in turn through orexin-1 receptor signaling in the ventral tegmental area and possibly other sites interfaces with the motivational and motor systems to increase intake of palatable food.

Key words: food intake; palatable food; high-fat diet; limbic system; nucleus accumbens; orexin-1 receptor

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Received Feb. 13, 2006; revised Aug. 25, 2007; accepted Aug. 25, 2007.

Correspondence should be addressed to Hans-Rudolf Berthoud, Pennington Biomedical Research Center, 6400 Perkins Road, Baton Rouge, LA 70808. Email: berthohr{at}pbrc.edu

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