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Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding

A number of studies have reported the involvement of the ventral hippocampus (vHip) and the lateral septum (LS) in negative emotional responses. Besides these well‐documented functions, they are also thought to control feeding behavior. In particular, optogenetic and pharmacogenetic interventions to...

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Detalles Bibliográficos
Autores principales: Kosugi, Kenzo, Yoshida, Keitaro, Suzuki, Toru, Kobayashi, Kenta, Yoshida, Kazunari, Mimura, Masaru, Tanaka, Kenji F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7984357/
https://www.ncbi.nlm.nih.gov/pubmed/33296119
http://dx.doi.org/10.1002/hipo.23289
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author Kosugi, Kenzo
Yoshida, Keitaro
Suzuki, Toru
Kobayashi, Kenta
Yoshida, Kazunari
Mimura, Masaru
Tanaka, Kenji F.
author_facet Kosugi, Kenzo
Yoshida, Keitaro
Suzuki, Toru
Kobayashi, Kenta
Yoshida, Kazunari
Mimura, Masaru
Tanaka, Kenji F.
author_sort Kosugi, Kenzo
collection PubMed
description A number of studies have reported the involvement of the ventral hippocampus (vHip) and the lateral septum (LS) in negative emotional responses. Besides these well‐documented functions, they are also thought to control feeding behavior. In particular, optogenetic and pharmacogenetic interventions to LS‐projecting vHip neurons have demonstrated that the vHip(→LS) neural circuit exerts an inhibition on feeding behavior. However, there have been no reports of vHip neuronal activity during feeding. Here, we focused on LS‐projecting vCA1 neurons (vCA1(→LS)) and monitored their activity during feeding behaviors in mice. vCA1(→LS) neurons were retrogradely labeled with adeno‐associated virus carrying a ratiometric Ca(2+) indicator and measured compound Ca(2+) dynamics by fiber photometry. We first examined vCA1(→LS) activity in random food‐exploring behavior and found that vCA1(→LS) activation seemed to coincide with food intake; however, our ability to visually confirm this during freely moving behaviors was not sufficiently reliable. We next examined vCA1(→LS) activity in a goal‐directed, food‐seeking lever‐press task which temporally divided the mouse state into preparatory, effort, and consummatory phases. We observed vCA1(→LS) activation in the postprandial period during the consummatory phase. Such timing‐ and pathway‐specific activation was not observed from pan‐vCA1 neurons. In contrast, reward omission eliminated this activity, indicating that vCA1(→LS) activation is contingent on the food reward. Sated mice pressed the lever significantly fewer times but still ate food; however, vCA1(→LS) neurons were not activated, suggesting that vCA1(→LS) neurons did not respond to habitual behavior. Combined, these results suggest that gastrointestinal interoception rather than food‐intake motions or external sensations are likely to coincide with vCA1(→LS) activity. Accordingly, we propose that vCA1(→LS) neurons discriminate between matched or unmatched predictive bodily states in which incoming food will satisfy an appetite. We also demonstrate that vCA1(→LS) neurons are activated in aversive/anxious situations in an elevated plus maze and tail suspension test. Future behavioral tests utilizing anxious conflict and food intake may reconcile the multiple functions of vCA1(→LS) neurons.
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spelling pubmed-79843572021-03-25 Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding Kosugi, Kenzo Yoshida, Keitaro Suzuki, Toru Kobayashi, Kenta Yoshida, Kazunari Mimura, Masaru Tanaka, Kenji F. Hippocampus Research Articles A number of studies have reported the involvement of the ventral hippocampus (vHip) and the lateral septum (LS) in negative emotional responses. Besides these well‐documented functions, they are also thought to control feeding behavior. In particular, optogenetic and pharmacogenetic interventions to LS‐projecting vHip neurons have demonstrated that the vHip(→LS) neural circuit exerts an inhibition on feeding behavior. However, there have been no reports of vHip neuronal activity during feeding. Here, we focused on LS‐projecting vCA1 neurons (vCA1(→LS)) and monitored their activity during feeding behaviors in mice. vCA1(→LS) neurons were retrogradely labeled with adeno‐associated virus carrying a ratiometric Ca(2+) indicator and measured compound Ca(2+) dynamics by fiber photometry. We first examined vCA1(→LS) activity in random food‐exploring behavior and found that vCA1(→LS) activation seemed to coincide with food intake; however, our ability to visually confirm this during freely moving behaviors was not sufficiently reliable. We next examined vCA1(→LS) activity in a goal‐directed, food‐seeking lever‐press task which temporally divided the mouse state into preparatory, effort, and consummatory phases. We observed vCA1(→LS) activation in the postprandial period during the consummatory phase. Such timing‐ and pathway‐specific activation was not observed from pan‐vCA1 neurons. In contrast, reward omission eliminated this activity, indicating that vCA1(→LS) activation is contingent on the food reward. Sated mice pressed the lever significantly fewer times but still ate food; however, vCA1(→LS) neurons were not activated, suggesting that vCA1(→LS) neurons did not respond to habitual behavior. Combined, these results suggest that gastrointestinal interoception rather than food‐intake motions or external sensations are likely to coincide with vCA1(→LS) activity. Accordingly, we propose that vCA1(→LS) neurons discriminate between matched or unmatched predictive bodily states in which incoming food will satisfy an appetite. We also demonstrate that vCA1(→LS) neurons are activated in aversive/anxious situations in an elevated plus maze and tail suspension test. Future behavioral tests utilizing anxious conflict and food intake may reconcile the multiple functions of vCA1(→LS) neurons. John Wiley & Sons, Inc. 2020-12-09 2021-03 /pmc/articles/PMC7984357/ /pubmed/33296119 http://dx.doi.org/10.1002/hipo.23289 Text en © 2020 The Authors. Hippocampus published by Wiley Periodicals LLC. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Kosugi, Kenzo
Yoshida, Keitaro
Suzuki, Toru
Kobayashi, Kenta
Yoshida, Kazunari
Mimura, Masaru
Tanaka, Kenji F.
Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding
title Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding
title_full Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding
title_fullStr Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding
title_full_unstemmed Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding
title_short Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding
title_sort activation of ventral ca1 hippocampal neurons projecting to the lateral septum during feeding
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7984357/
https://www.ncbi.nlm.nih.gov/pubmed/33296119
http://dx.doi.org/10.1002/hipo.23289
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