The Orexigenic Force of Olfactory Palatable Food Cues in Rats

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.

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The orexigenic force of olfactory palatable food cues in sated rats

10.1101/2021.07.06.451251 ◽

2021 ◽

Author(s):

Fiona Peris-Sampedro ◽

Iris Stoltenborg ◽

Marie V Le May ◽

Pol Sole-Navais ◽

Roger AH Adan ◽

...

Keyword(s):

Early Gene ◽

Male Rats ◽

Gene Marker ◽

Palatable Food ◽

Food Cues ◽

Ghrelin Receptor ◽

Hypothalamic Arcuate Nucleus ◽

Olfactory Detection ◽

Food Seeking ◽

External Stimuli

Background: Environmental cues recalling palatable foods are ubiquitous and motivate eating beyond metabolic need, yet the timing of this response and whether it can develop towards a non-palatable readily available food remain elusive. Although there is increasing evidence indicating that external stimuli in the olfactory modality can communicate with the major hub in the feeding neurocircuitry, the hypothalamic arcuate nucleus (Arc), the identity of hypothalamic substrates has been only partially uncovered. Methods: Using a palatable home-cage hidden-food paradigm, we investigate the ability of olfactory food cues to promote chow overconsumption in sated male rats, together with their impact on meal pattern. We likewise explore, by means of an immediate early gene marker, the neural mechanisms involved, including the possible engagement of the orexigenic ghrelin system. Results: Olfactory detection of a familiar palatable food shifts diurnal patterns towards an increase in meal frequency to cause persistent overconsumption of chow in sated conditions. In line with the orexigenic response observed, sensing the palatable food in the environment stimulates food-seeking and risk-taking behavior, and also triggers release of active ghrelin. Olfactory food cues recruit intermingled populations of cells embedded within the feeding circuitry within the Arc, including, notably, those containing the ghrelin receptor, even when food is not available for consumption. Conclusions: These data demonstrate 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.

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Central oxytocin signaling inhibits food reward-motivated behaviors and VTA dopamine responses to food-predictive cues in male rats

10.1101/2020.06.24.169540 ◽

2020 ◽

Author(s):

Clarissa M. Liu ◽

Ted M. Hsu ◽

Andrea N. Suarez ◽

Keshav S. Subramanian ◽

Ryan A. Fatemi ◽

...

Keyword(s):

Dopamine Neuron ◽

Dopamine Neurons ◽

Male Rats ◽

Target System ◽

Neuron Activity ◽

List Type ◽

Incentive Learning ◽

Palatable Food ◽

Reward Value ◽

Food Seeking

ABSTRACTOxytocin potently reduces food intake and is a potential target system for obesity treatment. A better understanding of the behavioral and neurobiological mechanisms mediating oxytocin’s anorexigenic effects may guide more effective obesity pharmacotherapy development. The present study examined the effects of central (lateral intracerebroventricular [ICV]) administration of oxytocin in rats on motivated responding for palatable food. Various conditioning procedures were employed to measure distinct appetitive behavioral domains, including food seeking in the absence of consumption (conditioned place preference expression), impulsive responding for food (differential reinforcement of low rates of responding), effort-based appetitive decision making (high-effort palatable vs. low-effort bland food), and postingestive reward value encoding (incentive learning). Results reveal that ICV oxytocin potently reduces food-seeking behavior, impulsivity, and effort-based palatable food choice, yet does not influence encoding of postingestive reward value in the incentive learning task. To investigate a potential neurobiological mechanism mediating these behavioral outcomes, we utilized in vivo fiber photometry in ventral tegmental area (VTA) dopamine neurons to examine oxytocin’s effect on phasic dopamine neuron responses to sucrose-predictive Pavlovian cues. Results reveal that ICV oxytocin significantly reduced food cue-evoked dopamine neuron activity. Collectively, these data reveal that central oxytocin signaling inhibits various obesity-relevant conditioned appetitive behaviors, potentially via reductions in food cue-driven phasic dopamine neural responses in the VTA.HighlightsCentral oxytocin inhibits motivated responding for palatable food reinforcementCentral oxytocin does not play a role in encoding postingestive reward valueCentral oxytocin blunts VTA dopamine neuron activity in response to food cues

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Stress induces compulsive palatable food seeking

Frontiers in Behavioral Neuroscience ◽

10.3389/conf.neuro.08.2009.09.213 ◽

2009 ◽

Vol 3 ◽

Author(s):

Ventura Rossella

Keyword(s):

Palatable Food ◽

Food Seeking

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Commentary: Gain in Body Fat Is Associated with Increased Striatal Response to Palatable Food Cues, whereas Body Fat Stability Is Associated with Decreased Striatal Response

Frontiers in Human Neuroscience ◽

10.3389/fnhum.2017.00065 ◽

2017 ◽

Vol 11 ◽

Author(s):

Silvia Cerolini ◽

Mariella Pazzaglia ◽

Caterina Lombardo

Keyword(s):

Body Fat ◽

Palatable Food ◽

Food Cues

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Dopamine D1-like receptors in prelimbic, but not infralimbic, medial prefrontal cortex contribute to chronic stress-induced increases in cue-induced relapse to palatable food seeking during forced abstinence

Behavioural Brain Research ◽

10.1016/j.bbr.2021.113583 ◽

2021 ◽

pp. 113583

Author(s):

Kevin T. Ball ◽

Guy M. Bennardo ◽

Jonathan Roe ◽

Kyle J. Wunderlich

Keyword(s):

Prefrontal Cortex ◽

Chronic Stress ◽

Medial Prefrontal Cortex ◽

Palatable Food ◽

Food Seeking

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Effects of chronic stress on reinstatement of palatable food seeking: Sex differences and relationship to trait anxiety

Physiology & Behavior ◽

10.1016/j.physbeh.2020.112900 ◽

2020 ◽

Vol 221 ◽

pp. 112900

Author(s):

Kevin T. Ball ◽

Olivia Best ◽

Erin Hagan ◽

Claire Pressimone ◽

Lindsay Tosh

Keyword(s):

Sex Differences ◽

Chronic Stress ◽

Trait Anxiety ◽

Palatable Food ◽

Food Seeking

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Sex Differences in Demand for Highly Palatable Foods: Role of the Orexin System

The International Journal of Neuropsychopharmacology ◽

10.1093/ijnp/pyaa040 ◽

2020 ◽

Cited By ~ 2

Author(s):

Linnea R Freeman ◽

Brandon S Bentzley ◽

Morgan H James ◽

Gary Aston-Jones

Keyword(s):

Sex Differences ◽

Demand Curve ◽

Female Rats ◽

Demand Elasticity ◽

Male Rats ◽

Neural Activation ◽

Palatable Food ◽

Behavioral Economic ◽

Male And Female Rats

Abstract Background The prevalence of eating disorders, including binge eating disorder, is significantly higher in women. These findings are mirrored by preclinical studies, which indicate that female rats have a higher preference for palatable food and show greater binge-like eating compared with male rats. Methods Here, we describe a novel within-session behavioral-economic paradigm that allows for the simultaneous measurement of the intake at null cost (Q0) and normalized demand elasticity (α) of 3 types of palatable food (low fat, high fat, and chocolate sucrose pellets) via demand curve analysis. In light of evidence that the orexin (hypocretin) system is critically involved in reward and feeding behaviors, we also examined the role of orexin function in sex differences of economic demand for palatable foods. Results The novel within-session behavioral-economic approach revealed that female rats have higher intake (demand) than males for all palatable foods at low cost (normalized to body weight) but no difference in intake at higher prices, indicating sex-dependent differences in the hedonic, but not motivational, aspects of palatable food. Immediately following behavioral-economic testing, we observed more orexin-expressing neurons and Fos expression (measure of recent neural activation) in these neurons in female rats compared with male rats. Moreover, the orexin-1 receptor antagonist SB334867 reduced both low- and high-cost intake for palatable food in both male and female rats. Conclusions These findings provide evidence of higher demand at low prices for palatable food in females and indicate that these behavioral differences may be associated with sexual dimorphism in orexin system function.

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Chronic restraint stress causes a delayed increase in responding for palatable food cues during forced abstinence via a dopamine D1-like receptor-mediated mechanism

Behavioural Brain Research ◽

10.1016/j.bbr.2016.11.020 ◽

2017 ◽

Vol 319 ◽

pp. 1-8 ◽

Cited By ~ 5

Author(s):

Kevin T. Ball ◽

Olivia Best ◽

Jonathan Luo ◽

Leah R. Miller

Keyword(s):

Restraint Stress ◽

Chronic Restraint Stress ◽

Palatable Food ◽

Food Cues

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Intrarenal Ghrelin Receptor Antagonism Prevents High-Fat Diet-Induced Hypertension in Male Rats

Endocrinology ◽

10.1210/en.2013-2177 ◽

2014 ◽

Vol 155 (7) ◽

pp. 2658-2666 ◽

Cited By ~ 6

Author(s):

Brandon A. Kemp ◽

Nancy L. Howell ◽

John J. Gildea ◽

Shetal H. Padia

Keyword(s):

Growth Hormone ◽

High Fat Diet ◽

Collecting Duct ◽

Male Rats ◽

Na Channel ◽

Standard Diet ◽

High Fat ◽

Ghrelin Receptor ◽

Induced Hypertension ◽

Epithelial Na Channel

Excess weight gain contributes up to 65% of the risk of primary hypertension, and the increase in blood pressure in response to high-fat diet (HFD) is preceded by significant increases in renal tubular sodium (Na+) reabsorption. In normal rats, intrarenal ghrelin infusion increases distal nephron-dependent Na+ reabsorption via activation of the intrarenal ghrelin receptor (GHSR). This study focusses on the role of intrarenal GHSR-mediated Na+ reabsorption in HFD-induced hypertension. Dahl salt-sensitive rats received standard diet or HFD for 6 weeks. Rats underwent uninephrectomy and osmotic minipump implantation for chronic intrarenal delivery of vehicle (0.25 μL/h × 28 d), selective GHSR antagonist [D-Lys-3]-growth hormone releasing peptide-6 (0.2μM/d), or GHSR inverse agonist [D-Arg1, D-Phe5, D-Trp7,9, Leu11]-substance P (SUB-P) (3.6μM/d). HFD rats with vehicle pumps had significantly increased renal GHSR expression compared with standard diet (0.092 ± 0.005 vs 0.065 ± 0.004 arbitrary units; P < .05), whereas acyl ghrelin levels were similar (16.3±6.2 vs 15.7±8.7 pg/g tissue). HFD rats with vehicle pumps became hypertensive after 2 weeks (P < .05) and showed a significant reduction in 24-hour urine Na+ before hypertension. At this time, these rats showed an increase in collecting duct α-epithelial Na+ channel, thereby providing a potential mechanism for the excess Na+ reabsorption. In contrast, HFD rats with [D-Lys-3]-growth hormone releasing peptide-6 or SUB-P pumps never became hypertensive and did not show the reduction in urine Na+. Because SUB-P blocks the constitutive, but not ghrelin-dependent, activity of the GHSR, and HFD-induced α-epithelial Na+ channel up-regulation was abolished during GHSR antagonism, these data suggest that HFD increases the constitutive activity of renal GHSR to increase Na+ reabsorption and induce hypertension in rats.

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