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The Journal of Neuroscience, September 7, 2005, 25(36):8295-8302; doi:10.1523/JNEUROSCI.2480-05.2005

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Behavioral/Systems/Cognitive
Amygdalar and Prefrontal Pathways to the Lateral Hypothalamus Are Activated by a Learned Cue That Stimulates Eating

Gorica D. Petrovich, Peter C. Holland, and Michela Gallagher

Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218

Experimental animals that are trained to associate a cue with food consumption when hunger prevails will subsequently consume a greater amount of food when that cue is presented under conditions of satiety. Previously, we showed that this phenomenon of conditioned potentiation of feeding is abolished by a neurotoxic lesion that encompasses the basolateral (BL), basomedial (BM), and lateral (LA) nuclei of the amygdala (AMY) and by disconnection of this region and lateral hypothalamus (LHA). Here, we combined immediate-early gene (IEG) and tract-tracing methods to map functional AMY–LHA circuitry that is engaged when potentiated feeding is produced by pavlovian conditioning. Sated rats were assessed for food consumption in the presence of a cue that was paired previously with food (CS+), or in the presence of another cue that was never paired with food (CS–), in two consecutive tests temporally arranged for activation of the effector IEGs Arc (activity-regulated cytoskeletal protein) and Homer 1a. We examined the selective induction of the IEGs by tests with CS+ or CS– presentations in AMY neurons that project to LHA, as identified with the retrograde tracer FluoroGold. Using the same labeling methods, we also examined neurons in several other forebrain regions, including the prefrontal cortex and nucleus accumbens, that receive strong inputs from BL/BM/LA nuclei and, in turn, innervate the LHA. Our results indicate that a cue that has acquired the ability to promote eating in sated rats (CS+) strongly activates a functional network formed by direct pathways from the BL/BM and orbitomedial prefrontal cortex to the LHA.

Key words: appetite; feeding; learning; pavlovian conditioning; satiation; network

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Received March 18, 2005; revised July 28, 2005; accepted August 3, 2005.

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