Food intake enhances hippocampal sharp wave-ripples

Effective regulation of energy metabolism is critical for survival. Metabolic control involves various nuclei within the hypothalamus, which receive information about the body’s energy state and coordinate appropriate responses to maintain homeostasis, such as thermogenesis, pancreatic insulin secre...

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Main Authors: Ekin Kaya, Evan Wegienka, Alexandra Akhtarzandi-Das, Hanh Do, Ada Eban-Rothschild, Gideon Rothschild
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-04-01
Series:eLife
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Online Access:https://elifesciences.org/articles/105059
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author Ekin Kaya
Evan Wegienka
Alexandra Akhtarzandi-Das
Hanh Do
Ada Eban-Rothschild
Gideon Rothschild
author_facet Ekin Kaya
Evan Wegienka
Alexandra Akhtarzandi-Das
Hanh Do
Ada Eban-Rothschild
Gideon Rothschild
author_sort Ekin Kaya
collection DOAJ
description Effective regulation of energy metabolism is critical for survival. Metabolic control involves various nuclei within the hypothalamus, which receive information about the body’s energy state and coordinate appropriate responses to maintain homeostasis, such as thermogenesis, pancreatic insulin secretion, and food-seeking behaviors. It has recently been found that the hippocampus, a brain region traditionally associated with memory and spatial navigation, is also involved in metabolic regulation. Specifically, hippocampal sharp wave-ripples (SWRs), which are high-frequency neural oscillations supporting memory consolidation and foraging decisions, have been shown to reduce peripheral glucose levels. However, whether SWRs are enhanced by recent feeding—when the need for glucose metabolism increases, and if so, whether feeding-dependent modulation of SWRs is communicated to other brain regions involved in metabolic regulation—remains unknown. To address these gaps, we recorded SWRs from the dorsal CA1 region of the hippocampus of mice during sleep sessions before and after consumption of meals of varying caloric values. We found that SWRs occurring during sleep are significantly enhanced following food intake, with the magnitude of enhancement being dependent on the caloric content of the meal. This pattern occurred under both food-deprived and ad libitum feeding conditions. Moreover, we demonstrate that GABAergic neurons in the lateral hypothalamus, which are known to regulate food intake, exhibit a robust SWR-triggered increase in activity. These findings identify the satiety state as a factor modulating SWRs and suggest that hippocampal-lateral hypothalamic communication is a potential mechanism by which SWRs could modulate peripheral metabolism and food intake.
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spelling doaj-art-d29b58bcc757441f87f0b5b9639de7f52025-08-20T03:06:43ZengeLife Sciences Publications LtdeLife2050-084X2025-04-011410.7554/eLife.105059Food intake enhances hippocampal sharp wave-ripplesEkin Kaya0https://orcid.org/0000-0001-9235-4954Evan Wegienka1Alexandra Akhtarzandi-Das2Hanh Do3Ada Eban-Rothschild4https://orcid.org/0000-0001-5816-1315Gideon Rothschild5https://orcid.org/0000-0002-9700-1020Department of Psychology, University of Michigan, Ann Arbor, United StatesDepartment of Psychology, University of Michigan, Ann Arbor, United StatesDepartment of Psychology, University of Michigan, Ann Arbor, United StatesDepartment of Psychology, University of Michigan, Ann Arbor, United StatesDepartment of Psychology, University of Michigan, Ann Arbor, United StatesDepartment of Psychology, University of Michigan, Ann Arbor, United States; Kresge Hearing Research Institute and Department of Otolaryngology, Head and Neck Surgery, University of Michigan, Ann Arbor, United StatesEffective regulation of energy metabolism is critical for survival. Metabolic control involves various nuclei within the hypothalamus, which receive information about the body’s energy state and coordinate appropriate responses to maintain homeostasis, such as thermogenesis, pancreatic insulin secretion, and food-seeking behaviors. It has recently been found that the hippocampus, a brain region traditionally associated with memory and spatial navigation, is also involved in metabolic regulation. Specifically, hippocampal sharp wave-ripples (SWRs), which are high-frequency neural oscillations supporting memory consolidation and foraging decisions, have been shown to reduce peripheral glucose levels. However, whether SWRs are enhanced by recent feeding—when the need for glucose metabolism increases, and if so, whether feeding-dependent modulation of SWRs is communicated to other brain regions involved in metabolic regulation—remains unknown. To address these gaps, we recorded SWRs from the dorsal CA1 region of the hippocampus of mice during sleep sessions before and after consumption of meals of varying caloric values. We found that SWRs occurring during sleep are significantly enhanced following food intake, with the magnitude of enhancement being dependent on the caloric content of the meal. This pattern occurred under both food-deprived and ad libitum feeding conditions. Moreover, we demonstrate that GABAergic neurons in the lateral hypothalamus, which are known to regulate food intake, exhibit a robust SWR-triggered increase in activity. These findings identify the satiety state as a factor modulating SWRs and suggest that hippocampal-lateral hypothalamic communication is a potential mechanism by which SWRs could modulate peripheral metabolism and food intake.https://elifesciences.org/articles/105059sharp wave-rippleshippocampusmetabolismhypothalamusfeeding
spellingShingle Ekin Kaya
Evan Wegienka
Alexandra Akhtarzandi-Das
Hanh Do
Ada Eban-Rothschild
Gideon Rothschild
Food intake enhances hippocampal sharp wave-ripples
eLife
sharp wave-ripples
hippocampus
metabolism
hypothalamus
feeding
title Food intake enhances hippocampal sharp wave-ripples
title_full Food intake enhances hippocampal sharp wave-ripples
title_fullStr Food intake enhances hippocampal sharp wave-ripples
title_full_unstemmed Food intake enhances hippocampal sharp wave-ripples
title_short Food intake enhances hippocampal sharp wave-ripples
title_sort food intake enhances hippocampal sharp wave ripples
topic sharp wave-ripples
hippocampus
metabolism
hypothalamus
feeding
url https://elifesciences.org/articles/105059
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AT hanhdo foodintakeenhanceshippocampalsharpwaveripples
AT adaebanrothschild foodintakeenhanceshippocampalsharpwaveripples
AT gideonrothschild foodintakeenhanceshippocampalsharpwaveripples