Abstract
Feeding behavior rarely occurs in direct response to metabolic deficit, yet the overwhelming majority of research on the biology of food intake control has focused on basic metabolic and homeostatic neurobiological substrates. Most animals, including humans, have habitual feeding patterns in which meals are consumed based on learned and/or environmental factors. Here we illuminate a novel neural system regulating higher-order aspects of feeding through which the gut-derived hormone ghrelin communicates with ventral hippocampus (vHP) neurons to stimulate meal-entrained conditioned appetite. Additional results show that the lateral hypothalamus (LHA) is a critical downstream substrate for vHP ghrelin-mediated hyperphagia and that vHP ghrelin activated neurons communicate directly with neurons in the LHA that express the neuropeptide, orexin. Furthermore, activation of downstream orexin-1 receptors is required for vHP ghrelin-mediated hyperphagia. These findings reveal novel neurobiological circuitry regulating appetite through which ghrelin signaling in hippocampal neurons engages LHA orexin signaling.
Highlights
Feeding behavior rarely occurs as a direct result of an immediate metabolic or nutrient deficiency
Ghrelin levels rise in anticipation of feeding (Frecka and Mattes, 2008; Cummings et al, 2001; Drazen et al, 2006) and ghrelin receptor null mice show blunted meal anticipatory responding under meal entrainment feeding schedules (Blum et al, 2009; Davis et al, 2011)
After exposure to a meal entrainment schedule in which rats were restricted to 4 hr food access each day, pharmacological blockade of ventral hippocampus (vHP) GHSR signaling prior to food access significantly reduced 4 hr chow consumption
Summary
Feeding behavior rarely occurs as a direct result of an immediate metabolic or nutrient deficiency. Environmental stimuli associated with learned meal anticipation elicit preparatory biological ‘cephalic’ responses (e.g., pancreatic insulin release) that occur prior to food consumption (Woods and Ramsay, 2000; Woods et al, 1970). These types of conditioned biological responses are advantageous when environmental factors place constraints on eating (e.g., predator threat, limited periods of food availability, and social or professional obligations) because they promote consumption of a large quantity of food within a relatively short time period. Genetic deletion of the ghrelin receptor (growth hormone secretagogue receptor 1A; GHSR) eliminates food anticipatory activity under meal entrainment feeding schedules
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