Hypothalamic interaction with reward-related regions during subjective evaluation of foods

The reward system implemented in the midbrain, ventral striatum, orbitofrontal cortex, and ventromedial prefrontal cortex evaluates and compares various types of rewards given to the organisms. It has been suggested that autonomic factors influence reward-related processing via the hypothalamus, but...

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Main Authors: Akitoshi Ogawa, Takahiro Osada, Masaki Tanaka, Akimitsu Suda, Koji Nakajima, Satoshi Oka, Koji Kamagata, Shigeki Aoki, Yasushi Oshima, Sakae Tanaka, Nobutaka Hattori, Seiki Konishi
Format: Article
Language:English
Published: Elsevier 2022-12-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922008655
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author Akitoshi Ogawa
Takahiro Osada
Masaki Tanaka
Akimitsu Suda
Koji Nakajima
Satoshi Oka
Koji Kamagata
Shigeki Aoki
Yasushi Oshima
Sakae Tanaka
Nobutaka Hattori
Seiki Konishi
author_facet Akitoshi Ogawa
Takahiro Osada
Masaki Tanaka
Akimitsu Suda
Koji Nakajima
Satoshi Oka
Koji Kamagata
Shigeki Aoki
Yasushi Oshima
Sakae Tanaka
Nobutaka Hattori
Seiki Konishi
author_sort Akitoshi Ogawa
collection DOAJ
description The reward system implemented in the midbrain, ventral striatum, orbitofrontal cortex, and ventromedial prefrontal cortex evaluates and compares various types of rewards given to the organisms. It has been suggested that autonomic factors influence reward-related processing via the hypothalamus, but how the hypothalamus modulates the reward system remains elusive. In this functional magnetic resonance imaging study, the hypothalamus was parcellated into individual hypothalamic nuclei performing different autonomic functions using boundary mapping parcellation analyses. The effective interaction during subjective evaluation of foods in a reward task was then investigated between the human hypothalamic nuclei and the reward-related regions. We found significant brain activity decrease in the paraventricular nucleus (PVH) and lateral nucleus in the hypothalamus in food evaluation compared with monetary evaluation. A psychophysiological interaction analysis revealed dual interactions between the PVH and (1) midbrain region and (2) ventromedial prefrontal cortex, with the former correlated with the stronger tendency of participants toward food-seeking. A dynamic causal modeling analysis further revealed unidirectional interactions from the PVH to the midbrain and ventromedial prefrontal cortex. These results suggest that the PVH in the human hypothalamus interacts with the reward-related regions in the cerebral cortex via multiple pathways (i.e., the midbrain pathway and ventromedial prefrontal pathway) to evaluate rewards for subsequent decision-making.
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spelling doaj.art-f7de1058dc7942ad935dd2a9a381da772022-12-22T03:00:19ZengElsevierNeuroImage1095-95722022-12-01264119744Hypothalamic interaction with reward-related regions during subjective evaluation of foodsAkitoshi Ogawa0Takahiro Osada1Masaki Tanaka2Akimitsu Suda3Koji Nakajima4Satoshi Oka5Koji Kamagata6Shigeki Aoki7Yasushi Oshima8Sakae Tanaka9Nobutaka Hattori10Seiki Konishi11Department of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, JapanDepartment of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, JapanDepartment of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, JapanDepartment of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Department of Neurology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, JapanDepartment of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Department of Orthopaedic Surgery, The University of Tokyo School of Medicine, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, JapanDepartment of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, JapanDepartment of Radiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, JapanDepartment of Radiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, JapanDepartment of Orthopaedic Surgery, The University of Tokyo School of Medicine, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, JapanDepartment of Orthopaedic Surgery, The University of Tokyo School of Medicine, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, JapanDepartment of Neurology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, JapanDepartment of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Research Institute for Diseases of Old Age, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Sportology Center, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Advanced Research Institute for Health Science, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Corresponding author at: Department of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.The reward system implemented in the midbrain, ventral striatum, orbitofrontal cortex, and ventromedial prefrontal cortex evaluates and compares various types of rewards given to the organisms. It has been suggested that autonomic factors influence reward-related processing via the hypothalamus, but how the hypothalamus modulates the reward system remains elusive. In this functional magnetic resonance imaging study, the hypothalamus was parcellated into individual hypothalamic nuclei performing different autonomic functions using boundary mapping parcellation analyses. The effective interaction during subjective evaluation of foods in a reward task was then investigated between the human hypothalamic nuclei and the reward-related regions. We found significant brain activity decrease in the paraventricular nucleus (PVH) and lateral nucleus in the hypothalamus in food evaluation compared with monetary evaluation. A psychophysiological interaction analysis revealed dual interactions between the PVH and (1) midbrain region and (2) ventromedial prefrontal cortex, with the former correlated with the stronger tendency of participants toward food-seeking. A dynamic causal modeling analysis further revealed unidirectional interactions from the PVH to the midbrain and ventromedial prefrontal cortex. These results suggest that the PVH in the human hypothalamus interacts with the reward-related regions in the cerebral cortex via multiple pathways (i.e., the midbrain pathway and ventromedial prefrontal pathway) to evaluate rewards for subsequent decision-making.http://www.sciencedirect.com/science/article/pii/S1053811922008655Dynamic causal modelingPsychophysiological interactionSubjective value
spellingShingle Akitoshi Ogawa
Takahiro Osada
Masaki Tanaka
Akimitsu Suda
Koji Nakajima
Satoshi Oka
Koji Kamagata
Shigeki Aoki
Yasushi Oshima
Sakae Tanaka
Nobutaka Hattori
Seiki Konishi
Hypothalamic interaction with reward-related regions during subjective evaluation of foods
NeuroImage
Dynamic causal modeling
Psychophysiological interaction
Subjective value
title Hypothalamic interaction with reward-related regions during subjective evaluation of foods
title_full Hypothalamic interaction with reward-related regions during subjective evaluation of foods
title_fullStr Hypothalamic interaction with reward-related regions during subjective evaluation of foods
title_full_unstemmed Hypothalamic interaction with reward-related regions during subjective evaluation of foods
title_short Hypothalamic interaction with reward-related regions during subjective evaluation of foods
title_sort hypothalamic interaction with reward related regions during subjective evaluation of foods
topic Dynamic causal modeling
Psychophysiological interaction
Subjective value
url http://www.sciencedirect.com/science/article/pii/S1053811922008655
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