Abstract
Environmental cues recalling palatable foods motivate eating beyond metabolic need, yet the timing of this response and whether it can develop towards a less palatable but readily available food remain elusive. Increasing evidence indicates that external stimuli in the olfactory modality communicate with the major hub in the feeding neurocircuitry, namely the hypothalamic arcuate nucleus (Arc), but the neural substrates involved have been only partially uncovered. By means of a home-cage hidden palatable food paradigm, aiming to mimic ubiquitous exposure to olfactory food cues in Western societies, we investigated whether the latter could drive the overeating of plain chow in non-food-deprived male rats and explored the neural mechanisms involved, including the possible engagement of the orexigenic ghrelin system. The olfactory detection of a familiar, palatable food impacted upon meal patterns, by increasing meal frequency, to cause the persistent overconsumption of chow. In line with the orexigenic response observed, sensing the palatable food in the environment stimulated food-seeking and risk-taking behavior, which are intrinsic components of food acquisition, and caused active ghrelin release. Our results suggest that olfactory food cues recruited intermingled populations of cells embedded within the feeding circuitry within the Arc, including, notably, those containing the ghrelin receptor. These data demonstrate the leverage of ubiquitous food cues, not only for palatable food searching, but also to powerfully drive food consumption in ways that resonate with heightened hunger, for which the orexigenic ghrelin system is implicated.
Highlights
Food cues in our environment are powerful triggers that encourage us to search for and consume food, even when there is no physiological need for it, standing as an important risk factor for obesity [1,2,3]
Our results suggest that these recruit intermingled populations of cells embedFos mapping, we identify the arcuate nucleus (Arc) as a key neural substrate activated by olfactory food ded within theresults feeding circuitry, chow nor the cued of PBcells are embedded available cues, and our suggest thateven thesewhen recruitneither intermingled populations for consumption
Previous work has shown that dopaminergic cells in the Arc respond to fasting and peripheral ghrelin, and, probably stand as a novel actor regulating energy homeostasis and food intake [26], our results suggest that these neuronal population might not be of critical relevance for integrating food-linked sensory stimuli in the olfactory modality
Summary
Food cues in our environment are powerful triggers that encourage us to search for and consume food, even when there is no physiological need for it, standing as an important risk factor for obesity [1,2,3]. Most studies exploring the mechanisms underpinning cue-potentiated feeding use classical Pavlovian conditioning models, in which animals learn through association that a nonfood stimulus (e.g., either discrete (a light or a tone) or contextual cues) signals food availability [4,5,6,7,8,9,10]. In nature, animals/humans mostly rely on the sense of smell or sight to perceive environmental food stimuli. It is well-known that the sense of smell is a central driver of food-seeking, appetite, and food preference in vertebrates, including humans [11,12], but one of those lingering questions in physiology research concerns the identification of the neural substrates involved in these feeding related outcomes. Control [13], and connections between the main olfactory bulb and the hypothalamic arcuate nucleus (Arc; a core hub in the feeding neurocircuitry) have been described [14,15].
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