Nucleus accumbens melanin-concentrating hormone signaling promotes feeding in a sex-specific manner

Terrill, Sarah J.; Subramanian, Keshav S.; Lan, Rae; Liu, Clarissa M.; Cortella, Alyssa M.; Noble, Emily E.; Kanoski, Scott E.

doi:10.1101/2020.06.16.155747

Cited by 4 publications

(7 citation statements)

References 61 publications

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“…To examine the role of CA1v to LS signaling on feeding behavior under free-feeding conditions, we examined meal pattern feeding analyses in the caspase vs. the control group (chronic CA1v-LS disconnection), and in the DREADDs group following CNO or vehicle (within-subjects design; reversible CA1v-LS disconnection). Results averaged over 5d revealed no significant effect of chronic shown that ICV CNO injections do not affect food intake in rats when tested under similar conditions (40). Collectively these findings show that reversible CA1v to LS disconnection increases food intake under free-feeding conditions, whereas food intake is not affected by chronic CA1v to LS ablation.…”

Section: Histological Analyses Confirmed Successful Viral Transfectiomentioning

confidence: 67%

“…3F&G). These results are unlikely based on nonselective effects of the CNO, as we've recently shown that ICV CNO injections do not affect food intake in rats when tested under similar conditions (37). Collectively these findings show that reversible CA1v to LS disconnection increases food intake under free-feeding conditions, whereas food intake is not affected by chronic CA1v to LS ablation.…”

Section: Histological Analyses Confirmed Successful Viral Transfection Of Ls-projecting Ca1vmentioning

confidence: 69%

“…Administration route for CNO (RTI International) and dosage were determined based on previous publications demonstrating reliable DREADDs activation (Hsu et al, 2018a; Noble et al, 2018; Terrill et al, 2020). Prior to behavioral testing where noted, all animals received an ICV 18mmol infusion (2uL total volume) of the DREADDs ligand clozapine N-oxide (CNO), rendering only DREADDs animals chemogenetically inactivated.…”

Section: Methods Detailsmentioning

confidence: 99%

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Ventral hippocampus-lateral septum circuitry promotes foraging-related memory

Davis

Liu

Gianatiempo

et al. 2020

Preprint

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Remembering the location of a food source is essential for securing energy for survival. 3Here we identify a hippocampal-septal neural circuit that controls food-directed spatial memory. 4Both reversible and chronic disconnection of ventral hippocampus CA1 subregion (CA1v) 5 projections to the lateral-septum (LS) using pathway-specific dual viral approaches impaired 6 memory retention in a spatial food-seeking foraging task in rats. However, disconnection of this 7 pathway did not affect performance in an aversive escape-motivated spatial memory task that 8 used the same apparatus and visuospatial cues, suggesting that CA1v-LS signaling selectively 9 mediates spatial memory for food location vs. spatial memory in general. The selectivity of this 10 pathway in mediating foraging-related spatial memory was further supported by results showing 11 that CA1v-LS disconnection did not affect anxiety-like behavior, locomotor activity, or social 12 and olfactory-based appetitive learning. To examine whether CA1v-LS mediation of foraging-13 related spatial memory involves collateral projections of CA1v neurons, we utilized virus-based 14 neural pathway tracing analyses to identify the mPFC as a collateral target of LS-projecting 15 CA1v neurons. However, functional disconnection of the CA1v and mPFC did not affect spatial 16 memory for food location, thus further supporting the selectivity of CA1v-LS signaling for this 17 behavior. The nucleus accumbens, lateral hypothalamic area, and other brain regions associated 18 with food motivation and reward were identified as second-order targets of CA1v-LS signaling 19 using a multisynaptic anterograde tracing approach. Collective results reveal that CA1v to LS 20 communication plays a critical role in remembering the environmental location of food, thus 21 identifying a novel neural pathway regulating foraging-related memory processes. 22 23 24 25 26 27 28 29 30 31(temporal pole; HPCv), while classically associated with stress-and affect-associated memory 55 processes (7), also plays a role in visuospatial learning and memory (8-10). For example, under 56 some testing conditions selective HPCv lesions impair spatial memory performance in the Morris 57 water maze (10, 11). Moreover, place cells that are responsive to changes in the visuospatial 58 environment are present within both the HPCd and HPCv pyramidal layers, with a linear 59 increase in the scale of representation from the dorsal to the ventral pole (9). Despite a common 60 role for the HPCd and HPCv in mediating spatial memory, there is also evidence for a functional 61 distinction between the subregions (7, 12, 13). For instance, lesions of the HPCv but not the 62 HPCd alter stress responses (14) and anxiety-like behavior (15), whereas HPCd but not HPCv 63 lesions impair spatial memory in an incidental (nonreinforced) procedure (16). These two HPC 64 subregions also have distinct afferent and efferent neural connections. This disparate 65 neuroanatomical connectivity supports a framework for a functional diversity in ...

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Section: Histological Analyses Confirmed Successful Viral Transfectiomentioning

confidence: 67%

Section: Histological Analyses Confirmed Successful Viral Transfection Of Ls-projecting Ca1vmentioning

confidence: 69%

Section: Methods Detailsmentioning

confidence: 99%

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Ventral hippocampus-lateral septum circuitry promotes foraging-related memory

Davis

Liu

Gianatiempo

et al. 2020

Preprint

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“…The same population of ORX neurons projects to the ACBsh and PVT (Lee and Lee 2016). In terms of sex speci c behavioral networks, the ACB shell is where the lateral hypothalamic hunger peptide MCH neurons were shown to promote a male-speci c increase in consumption of chow and palatable foods (Terrill et al 2020).…”

Section: The Nucleus Accumbensmentioning

confidence: 99%

Sex Differences in Activation of Forebrain Orexin Targets During Hedonic Eating

Parsons

Greiner

Buczek

et al. 2022

Preprint

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Palatable foods can stimulate appetite without hunger, and unconstrained overeating underlies obesity and binge eating disorder. Women are more prone to obesity and binge eating than men but the neural causes of individual differences are unknown. In an animal model of hedonic eating, a prior study found that females were more susceptible than males to eat palatable food when sated and that the neuropeptide orexin/hypocretisn (ORX) was crucial in both sexes. The current study examined potential forebrain targets of ORX signaling during hedonic eating. We measured Fos induction in the cortical, thalamic, striatal, and amygdalar areas that receive substantial ORX inputs and contain their receptors in hungry and sated male and female rats during consumption of a palatable (high-sucrose) food. During the test, hungry rats of both sexes ate substantial amounts, and while sated males ate much less than hungry rats, sated females ate as much as hungry rats. The Fos induction analysis identified sex differences in recruitment of specific areas of the medial prefrontal cortex (mPFC), paraventricular nucleus of the thalamus (PVT), nucleus accumbens (ACB), and central nucleus of the amygdala (CEA), and similar patterns across sexes in the insular cortex and areas of the ACB and CEA. There was a striking activation of the mPFC in sated males, who consumed the least amount food and unique correlations between the PVT and the CEA in females and the PVT and ACB in males. The study identified key functional circuits that may drive hedonic eating in a sex specific manner.

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“…The role of coexpressed glutamate may support MCH‐mediated functions, including well‐established roles in the regulation of energy balance. Acute central MCH administration, 10 activation of MCH neurons, 11 or activation of the MCH receptor (MCHR1) stimulates feeding, 12‐14 and chronic MCH administration can promote body weight gain 15 . By contrast, mice that lack MCH or MCHR1 are lean, hyperactive and have increased energy expenditure 16‐18 .…”

Section: Introductionmentioning

confidence: 99%

Loss of glutamatergic signalling from MCH neurons reduced anxiety‐like behaviours in novel environments

Sankhe

Bordeleau

Alfonso

et al. 2022

J Neuroendocrinology

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Melanin‐concentrating hormone (MCH) neurons within the hypothalamus are heterogeneous and can coexpress additional neuropeptides and transmitters. The majority of MCH neurons express vesicular transporters to package glutamate for synaptic release, and MCH neurons can directly innervate downstream neurons via glutamate release. Although glutamatergic signalling from MCH neurons may support physiological and behavioural roles that are independent of MCH (e.g., in glucose homeostasis and nutrient‐sensing), it can also mediate similar roles to MCH in the regulation of energy balance. In addition to energy balance, the MCH system has also been implicated in mood disorders, as MCH receptor antagonists have anxiolytic and anti‐depressive effects. However, the contribution of glutamatergic signalling from MCH neurons to mood‐related functions have not been investigated. We crossed Mch‐cre mice with floxed‐Vglut2 mice to delete the expression of the vesicular glutamate transporter 2 (Vglut2) and disable glutamatergic signalling specifically from MCH neurons. The resulting Mch‐Vglut2‐KO mice showed Vglut2 deletion from over 75% of MCH neurons, and although we did not observe changes in depressive‐like behaviours, we found that Mch‐Vglut2‐KO mice displayed anxiety‐like behaviours. Mch‐Vglut2‐KO mice showed reduced exploratory activity when placed in a new cage and were quicker to consume food placed in the centre of a novel open arena. These findings showed that Vglut2 deletion from MCH neurons resulted in anxiolytic actions and suggested that the anxiogenic effects of glutamate are similar to those of the MCH peptide. Taken together, these findings suggest that glutamate and MCH may synergize to regulate and promote anxiety‐like behaviour.

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Nucleus accumbens melanin-concentrating hormone signaling promotes feeding in a sex-specific manner

Cited by 4 publications

References 61 publications

Ventral hippocampus-lateral septum circuitry promotes foraging-related memory

Ventral hippocampus-lateral septum circuitry promotes foraging-related memory

Sex Differences in Activation of Forebrain Orexin Targets During Hedonic Eating

Loss of glutamatergic signalling from MCH neurons reduced anxiety‐like behaviours in novel environments

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