Ventral hippocampus-lateral septum circuitry promotes foraging-related memory

Décarie-Spain, Léa; Liu, Clarissa M.; Lauer, Logan Tierno; Subramanian, Keshav S.; Bashaw, Alexander G.; Klug, Molly E.; Gianatiempo, Isabella H.; Suarez, Andrea N.; Noble, Emily E.; Donohue, Kristen N.; Cortella, Alyssa M.; Hahn, Joel D.; Davis, Elizabeth A.; Kanoski, Scott E.

doi:10.1016/j.celrep.2022.111402

Cited by 21 publications

(20 citation statements)

References 76 publications

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“…4b, c). We have previously shown that LV infusion of CNO in the absence of hM4Di receptors does not impact performance in this task 31 . Thus, CA1v meal-responsive neurons promote foraging-related spatial memory through a CA1v-to-LHA signaling pathway.…”

Section: Resultsmentioning

confidence: 86%

“…To assess the selectivity of CA1v meal-responsive neurons in mediating meal-related spatial memory (vs. spatial memory in general), another cohort of animals underwent the same meal-related ablation or control treatment as the previous cohort, before training in an escape-based spatial memory task (Fig. 2h) that employs the same apparatus as the foraging version and is of similar difficulty, but without food reinforcement 31 . In this case, Fed rats did not differ from ‘Control’ animals during escape location training (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…That HPCv neurons are engaged upon food consumption is consistent with previous studies revealing that optogenetic inhibition of HPCv neurons influences food intake 16,34,37 . Further, fiber photometry recordings of HPCv calcium-dependent activity reveal dynamic changes during foraging and food-seeking behaviors 31,33 . Our present results advance these findings by establishing a role for HPCv neuronal activity during eating behaviors in encoding meal-related memory, thus providing a mechanistic framework for this previous literature.…”

Section: Discussionmentioning

confidence: 99%

“…For the test session, rats were placed in the chambers to lever press for sucrose under a progressive ratio reinforcement schedule. The response requirement increased progressively using the following formula: F(i) = 5eˆ0.2i-5, where F(i) is the number of lever presses required for the next pellet at i = pellet number and the breakpoint was defined as the final completed lever press requirement that preceded a 20-min period without earning a reinforcer, as described previously 12,31 .…”

Section: Effort-based Lever Pressingmentioning

confidence: 99%

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Ventral hippocampus neurons encode meal-related memory

Décarie-Spain,

Gu,

Lauer

et al. 2023

Preprint

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The ability to encode and retrieve meal-related information is critical to efficiently guide energy acquisition and consumption, yet the underlying neural processes remain elusive. Here we reveal that ventral hippocampus (HPCv) neuronal activity dynamically elevates during meal consumption and this response is highly predictive of subsequent performance in a foraging-related spatial memory task. Targeted recombination-mediated ablation of HPCv meal-responsive neurons impairs foraging-related spatial memory without influencing food motivation, anxiety-like behavior, or escape-mediated spatial memory. These HPCv meal-responsive neurons project to the lateral hypothalamic area (LHA) and single-nucleus RNA sequencing and in situ hybridization analyses indicate they are enriched in serotonin 2a receptors (5HT2aR). Either chemogenetic silencing of HPCv-to-LHA projections or intra-HPCv 5HT2aR antagonist yielded foraging-related spatial memory deficits, as well as alterations in caloric intake and the temporal sequence of spontaneous meal consumption. Collective results identify a population of HPCv neurons that dynamically respond to eating to encode meal-related memories.

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Section: Resultsmentioning

confidence: 86%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Effort-based Lever Pressingmentioning

confidence: 99%

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Ventral hippocampus neurons encode meal-related memory

Décarie-Spain,

Gu,

Lauer

et al. 2023

Preprint

Self Cite

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“…Olfactory cues are often used in spatial navigation and food or food cues are often used to guide spatial exploration tasks 45, 46 . To assess whether OB GHSR contribute to spatial exploration and learning, we used a Y maze and radial arm maze (RAM).…”

Section: Resultsmentioning

confidence: 99%

Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism

Stark

Dempsey

Sassi

et al. 2023

Preprint

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Growing evidence highlights a complex interaction between olfaction and metabolism with impaired olfactory function observed in obesity and increased olfactory sensitivity during hunger. The mechanisms linking metabolic state and olfaction remain unknown, but increased accessibility of hormones, such as ghrelin, and the diverse expression of hormone receptors such as those for ghrelin (GHSRs) in the olfactory system suggests an underappreciated neuroendocrine role. Here, we examined the hypothesis that GHSRs in the olfactory bulb (OB) link hunger with olfactory sensitivity to influence foraging behaviours and metabolism. Selective deletion of OBGHSRs in adult male mice was achieved with adeno-associated viral expression of cre-recombinase in the OB of floxed-Ghsr mice. OBGHSR deletion significantly affected olfactory discrimination and habituation to both food and pheromone odours, with greatest effect under fasted conditions. Anxiety-like and depression-like behaviour was significantly greater after OBGHSR deletion using 3 independent anxiety behavioural tasks and testing for anhedonia, whereas exploratory behaviour was reduced. No effect on spatial navigation and memory was observed. Although OBGHSR deletion did not affect cumulative food intake, it significantly impacted feeding behaviour as evidenced by altered bout number and duration. Moreover, food-finding after fasting or ip ghrelin was attenuated. Intriguingly, OBGHSR deletion caused an increase in body weight and fat mass, spared fat utilisation on a chow diet and impaired glucose metabolism indicating metabolic dysfunction. We conclude that OBGHSRs maintain olfactory sensitivity, particularly during hunger, and facilitate behavioural adaptations that optimise food-seeking in anxiogenic environments, priming metabolic pathways in preparation for food consumption.

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Obesity‐ and diet‐induced plasticity in systems that control eating and energy balance

Ferrario,

Münzberg‐Gruening,

Rinaman

et al. 2024

Obesity

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In April 2023, the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), in partnership with the National Institute of Child Health and Human Development, the National Institute on Aging, and the Office of Behavioral and Social Sciences Research, hosted a 2‐day online workshop to discuss neural plasticity in energy homeostasis and obesity. The goal was to provide a broad view of current knowledge while identifying research questions and challenges regarding neural systems that control food intake and energy balance. This review includes highlights from the meeting and is intended both to introduce unfamiliar audiences with concepts central to energy homeostasis, feeding, and obesity and to highlight up‐and‐coming research in these areas that may be of special interest to those with a background in these fields. The overarching theme of this review addresses plasticity within the central and peripheral nervous systems that regulates and influences eating, emphasizing distinctions between healthy and disease states. This is by no means a comprehensive review because this is a broad and rapidly developing area. However, we have pointed out relevant reviews and primary articles throughout, as well as gaps in current understanding and opportunities for developments in the field.

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Ventral hippocampus-lateral septum circuitry promotes foraging-related memory

Cited by 21 publications

References 76 publications

Ventral hippocampus neurons encode meal-related memory

Ventral hippocampus neurons encode meal-related memory

Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism

Obesity‐ and diet‐induced plasticity in systems that control eating and energy balance

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