Sex differences in activation of extra-hypothalamic forebrain areas during hedonic eating

Parsons, W. Shelby; Greiner, Eliza M.; Buczek, Laura; Migliaccio, Jennifer; Corbett, Erin; Madden, Amanda M. K.; Petrovich, Gorica D.

doi:10.1007/s00429-022-02580-0

Cited by 7 publications

(5 citation statements)

References 48 publications

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“…One recent study showed activation of PVT in response to hedonic feeding in sated females but not males. Of note, the same sex difference was not observed in insula [ 62 ]. Further, stress-induced electrophysiological changes in PVT neurons are observed in males but not females, providing a possible mechanism underlying the impairment in habituation to restraint stress observed in females [ 63 ].…”

Section: Discussionmentioning

confidence: 77%

A paraventricular thalamus to insular cortex glutamatergic projection gates “emotional” stress-induced binge eating in females

Anversa

Campbell

Ch’ng

et al. 2023

Neuropsychopharmacol.

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It is well-established that stress and negative affect trigger eating disorder symptoms and that the brains of men and women respond to stress in different ways. Indeed, women suffer disproportionately from emotional or stress-related eating, as well as associated eating disorders such as binge eating disorder. Nevertheless, our understanding of the precise neural circuits driving this maladaptive eating behavior, particularly in women, remains limited. We recently established a clinically relevant model of ‘emotional’ stress-induced binge eating whereby only female mice display binge eating in response to an acute “emotional” stressor. Here, we combined neuroanatomic, transgenic, immunohistochemical and pathway-specific chemogenetic approaches to investigate whole brain functional architecture associated with stress-induced binge eating in females, focusing on the role of Vglut2 projections from the paraventricular thalamus (PVTVglut2+) to the medial insular cortex in this behavior. Whole brain activation mapping and hierarchical clustering of Euclidean distances revealed distinct patterns of coactivation unique to stress-induced binge eating. At a pathway-specific level, PVTVglut2+ cells projecting to the medial insular cortex were specifically activated in response to stress-induced binge eating. Subsequent chemogenetic inhibition of this pathway suppressed stress-induced binge eating. We have identified a distinct PVTVglut2+ to insular cortex projection as a key driver of “emotional” stress-induced binge eating in female mice, highlighting a novel circuit underpinning this sex-specific behavior.

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Section: Discussionmentioning

confidence: 77%

A paraventricular thalamus to insular cortex glutamatergic projection gates “emotional” stress-induced binge eating in females

Anversa

Campbell

Ch’ng

et al. 2023

Neuropsychopharmacol.

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“…Sex dependent neural differences in Fos induction were previously found in the CEAm based on deprivation state ( Parsons et al, 2022 ), and food deprivation recruits the ACB in both sexes. ( Parsons et al, 2022 ; Carr, 2011 ).…”

Section: Sex Differencesmentioning

confidence: 75%

“…Male and female rodents differ in their physiological responses to food restriction (Kane et al, 2018). Sex dependent neural differences in Fos induction were previously found in the CEAm based on deprivation state (Parsons et al, 2022), and food deprivation recruits the ACB in both sexes. (Parsons et al, 2022;Carr, 2011).…”

Section: Sex Differencesmentioning

confidence: 78%

“…The novel food (TestDiet pellets) used in the current study is high in sucrose, and therefore more palatable than the familiar food (Rat Chow). Palatable foods were previously shown to increase Fos induction in the CEA ( Park & Carr, 1998 , Wu et al, 2014 ; Parsons et al, 2022 ) and a subset of CEA neurons that express prepronociceptin (CEA Pnoc ) mediate palatable food consumption ( Hardaway et al, 2019 ). These CEA Pnoc neurons are located predominantly in the CEAm and CEAl ( Hardaway et al, 2019 ), and their inhibition reduced the latency to feed in a novel environment as well as consumption in home cage after novelty exposure ( Hardaway et al, 2019 ).…”

Section: Novel Foodmentioning

confidence: 99%

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Activation patterns in male and female forebrain circuitries during food consumption under novelty

Greiner,

Witt,

Moran

et al. 2023

Preprint

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The influence of novelty on feeding behavior is significant and can override both homeostatic and hedonic drives due to the uncertainty of potential danger. Previous work found that novel food hypophagia is enhanced in a novel environment and that males habituate faster than females. The current study’s aim was to identify the neural substrates of separate effects of food and context novelty. Adult male and female rats were tested for consumption of a novel or family food in either a familiar or in a novel context. Test-induced Fos expression was measured in the amygdalar, thalamic, striatal, and prefrontal cortex regions that are important for appetitive responding, contextual processing, and reward motivation. Food and context novelty induced strikingly different activation patterns. Novel context induced Fos robustly in almost every region analyzed, including the central (CEA) and basolateral complex nuclei of the amygdala, the thalamic paraventricular (PVT) and reuniens nuclei, the nucleus accumbens (ACB), the medial prefrontal cortex prelimbic and infralimbic areas, and the dorsal agranular insular cortex (AI). Novel food induced Fos in a few select regions: the CEA, anterior basomedial nucleus of the amygdala, anterior PVT, and posterior AI. There were also sex differences in activation patterns. The capsular and lateral CEA had greater activation for male groups and the anterior PVT, ACB ventral core and shell had greater activation for female groups. These activation patterns and correlations between regions, suggest that distinct functional circuitries control feeding behavior when food is novel and when eating occurs in a novel environment.

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“…Finally, given that we now identified hedonic overdrive as a key feature driving male mouse overconsumption when exposed to high‐fat diets, why female C57BL/6 mice do not have the same magnitude of response as males would seem a profitable area for future investigation. This is particularly the case because some studies have suggested that female rats may be more susceptible to hedonic eating when sated than males [52, 53]. The molecular basis of what happens in the brains of mice during the different phases of response after high‐fat diet exposure would seem a profitable area of future investigation.…”

Section: Discussionmentioning

confidence: 99%

The hedonic overdrive model best explains high‐fat diet‐induced obesity in C57BL/6 mice

Gao,

Hu,

Yang

et al. 2024

Obesity

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ObjectiveHigh‐fat diets cause obesity in male mice; however, the underlying mechanisms remain controversial. Here, three contrasting ideas were assessed: hedonic overdrive, reverse causality, and passive overconsumption models.MethodsA total of 12 groups of 20 individually housed 12‐week‐old C57BL/6 male mice were exposed to 12 high‐fat diets with varying fat content from 40% to 80% (by calories), protein content from 5% to 30%, and carbohydrate content from 8.4% to 40%. Body weight and food intake were monitored for 30 days after 7 days at baseline on a standard low‐fat diet.ResultsAfter exposure to the diets, energy intake increased first, and body weight followed later. Intake then declined. The peak energy intake was dependent on both dietary protein and carbohydrate, but not the dietary fat and energy density, whereas the rate of decrease in intake was only related to dietary protein. On high‐fat diets, the weight of food intake declined, but despite this average reduction of 14.4 g in food intake, they consumed, on average, 357 kJ more energy than at baseline.ConclusionsThe hedonic overdrive model fit the data best. The other two models were not supported.

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Sex differences in activation of extra-hypothalamic forebrain areas during hedonic eating

Cited by 7 publications

References 48 publications

A paraventricular thalamus to insular cortex glutamatergic projection gates “emotional” stress-induced binge eating in females

A paraventricular thalamus to insular cortex glutamatergic projection gates “emotional” stress-induced binge eating in females

Activation patterns in male and female forebrain circuitries during food consumption under novelty

The hedonic overdrive model best explains high‐fat diet‐induced obesity in C57BL/6 mice

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