Hippocampal neurons inhibit meal onset

Abstract

There is extensive research regarding the neural mechanisms involved in satiety and meal termination; in contrast, there is very limited understanding of how meal onset is regulated. On the basis of several converging lines of evidence, we hypothesized that hippocampal neurons form a memory of a meal and inhibit meal onset during the postprandial period. As a first step, we tested whether reversible inactivation of the hippocampus with muscimol infusions after the end of one meal would accelerate the onset of the next meal. To test this, adult male Sprague-Dawley rats (N = 23) were implanted with a cannula aimed at the right or left dorsal hippocampus and then trained to consume a 32% sucrose solution at a scheduled time daily. On the experimental day, hippocampal neuronal activity was temporarily disrupted during the postprandial period by infusing muscimol (0.5 μg/μl; 1 μl) 5 min after the rats stopped consuming the sucrose solution. Compared to vehicle infusions, muscimol infusions significantly decreased the latency to start the postinfusion meal and increased the size of the postinfusion meal. In addition, muscimol disrupted the relationship between the size of a meal and length of the following postprandial period. These effects of muscimol on meal onset were not due to an effect on the speed of consumption. Collectively, these findings are consistent with the hypothesis that hippocampal neurons suppress meal initiation during the postprandial period. Given that overeating can impair hippocampal function, these findings suggest that impaired hippocampal functioning is a cause and consequence of overeating and obesity.

The anterior medial temporal lobes: Their role in food intake and body weight regulation

“…Additionally, glucagon-like peptide-I (GLP-I) receptors in the ventral hippocampus also influence food intake and willingness to work to obtain food (i.e., "wanting"; [65,81]). Furthermore, there is solid evidence showing that hippocampal neurons form a memory of a meal and inhibit meal onset after a meal has been consumed [53,115,117]. These findings show that the hippocampus is a very likely target of the modulation exerted by interoceptive signal of hunger and satiety.…”

“…In line with this notion, Huff, Emmons, Narayanan, & LaLumiere [68] have shown that the basolateral amygdala interacts with the ventral hippocampus to modulate specific types of learning (e.g., footshock learning) but not others (here context learning). This is also suggests that similarly, the hippocampus may not be one entity (e.g., [36,53,85,101]). For instance, while the ventral hippocampus has bi-directional connections to the amygdala, the dorsal hippocampus does not have any [33].…”

Hippocampus Contributions to Food Intake Control: Mnemonic, Neuroanatomical, and Endocrine Mechanisms

“…Parent and colleagues recently examined the impact of postprandial inactivation of hippocampal neurons on subsequent feeding behavior (21). After rats were trained to reliably and rapidly consume a 32% sucrose solution at a scheduled time daily, reversible inactivation of dorsal hippocampal neurons (via parenchymal GABA receptor agonist infusion) immediately following sucrose consumption decreased the latency to initiate feeding and increased the size of the subsequent chow meal.…”

The outward spiral: a vicious cycle model of obesity and cognitive dysfunction

“…For example, temporary inactivation of the dorsal hippocampus in rats decreases intermeal intervals [27], suggesting a diminished capacity for satiety signals to inhibit intake during the period following a meal. Furthermore, the conversion of circulating triglycerides to fatty acids increases following food intake, providing a source of satiety signals detectable in the brain [28].…”