Emotion in action: When emotions meet motor circuits
The brain is a remarkably complex organ responsible for a wide range of functions, including the modulation of emotional states and movement. Neuronal circuits are believed to play a crucial role in integrating sensory, cognitive, and emotional information to ultimately guide motor behavior. Over th...
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Veröffentlicht in: | Neuroscience and biobehavioral reviews 2023-12, Vol.155, p.105475-105475, Article 105475 |
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description | The brain is a remarkably complex organ responsible for a wide range of functions, including the modulation of emotional states and movement. Neuronal circuits are believed to play a crucial role in integrating sensory, cognitive, and emotional information to ultimately guide motor behavior. Over the years, numerous studies employing diverse techniques such as electrophysiology, imaging, and optogenetics have revealed a complex network of neural circuits involved in the regulation of emotional or motor processes. Emotions can exert a substantial influence on motor performance, encompassing both everyday activities and pathological conditions. The aim of this review is to explore how emotional states can shape movements by connecting the neural circuits for emotional processing to motor neural circuits. We first provide a comprehensive overview of the impact of different emotional states on motor control in humans and rodents. In line with behavioral studies, we set out to identify emotion-related structures capable of modulating motor output, behaviorally and anatomically. Neuronal circuits involved in emotional processing are extensively connected to the motor system. These circuits can drive emotional behavior, essential for survival, but can also continuously shape ongoing movement. In summary, the investigation of the intricate relationship between emotion and movement offers valuable insights into human behavior, including opportunities to enhance performance, and holds promise for improving mental and physical health. This review integrates findings from multiple scientific approaches, including anatomical tracing, circuit-based dissection, and behavioral studies, conducted in both animal and human subjects. By incorporating these different methodologies, we aim to present a comprehensive overview of the current understanding of the emotional modulation of movement in both physiological and pathological conditions.
•Emotions significantly influence motor performance in daily activities and pathological conditions.•Numerous emotion-related structures are mono-synaptically connected to motor circuits.•Most manipulations of emotion-related structures impact motor behavior.•Neural networks for emotional modulation of movement include limbic system and motor-related regions•Studying emotion-motor circuit connectivity in animals offers insights into human physiopathology. |
doi_str_mv | 10.1016/j.neubiorev.2023.105475 |
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•Emotions significantly influence motor performance in daily activities and pathological conditions.•Numerous emotion-related structures are mono-synaptically connected to motor circuits.•Most manipulations of emotion-related structures impact motor behavior.•Neural networks for emotional modulation of movement include limbic system and motor-related regions•Studying emotion-motor circuit connectivity in animals offers insights into human physiopathology.</description><identifier>ISSN: 0149-7634</identifier><identifier>EISSN: 1873-7528</identifier><identifier>DOI: 10.1016/j.neubiorev.2023.105475</identifier><identifier>PMID: 37996047</identifier><language>eng</language><publisher>United States: Elsevier Ltd</publisher><subject>Animals ; Basal ganglia ; Brain ; Brain - physiology ; Emotional states ; Emotions - physiology ; Humans ; Life Sciences ; Limbic system ; Motor behavior ; Motor system ; Movement ; Movement - physiology ; Neuromodulators ; Neuronal circuits ; Neurons ; Neurons and Cognition ; Psychology and behavior ; Sensory-motor control</subject><ispartof>Neuroscience and biobehavioral reviews, 2023-12, Vol.155, p.105475-105475, Article 105475</ispartof><rights>2023 The Authors</rights><rights>Copyright © 2023 The Authors. Published by Elsevier Ltd.. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c466t-8048d95ec39c877b1d0e2ccbe3ad2f9248fbcd4accd555eb3d442aa5b940913f3</cites><orcidid>0000-0002-2628-2638</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S014976342300444X$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37996047$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04311811$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Braine, Anaelle</creatorcontrib><creatorcontrib>Georges, François</creatorcontrib><title>Emotion in action: When emotions meet motor circuits</title><title>Neuroscience and biobehavioral reviews</title><addtitle>Neurosci Biobehav Rev</addtitle><description>The brain is a remarkably complex organ responsible for a wide range of functions, including the modulation of emotional states and movement. Neuronal circuits are believed to play a crucial role in integrating sensory, cognitive, and emotional information to ultimately guide motor behavior. Over the years, numerous studies employing diverse techniques such as electrophysiology, imaging, and optogenetics have revealed a complex network of neural circuits involved in the regulation of emotional or motor processes. Emotions can exert a substantial influence on motor performance, encompassing both everyday activities and pathological conditions. The aim of this review is to explore how emotional states can shape movements by connecting the neural circuits for emotional processing to motor neural circuits. We first provide a comprehensive overview of the impact of different emotional states on motor control in humans and rodents. In line with behavioral studies, we set out to identify emotion-related structures capable of modulating motor output, behaviorally and anatomically. Neuronal circuits involved in emotional processing are extensively connected to the motor system. These circuits can drive emotional behavior, essential for survival, but can also continuously shape ongoing movement. In summary, the investigation of the intricate relationship between emotion and movement offers valuable insights into human behavior, including opportunities to enhance performance, and holds promise for improving mental and physical health. This review integrates findings from multiple scientific approaches, including anatomical tracing, circuit-based dissection, and behavioral studies, conducted in both animal and human subjects. By incorporating these different methodologies, we aim to present a comprehensive overview of the current understanding of the emotional modulation of movement in both physiological and pathological conditions.
•Emotions significantly influence motor performance in daily activities and pathological conditions.•Numerous emotion-related structures are mono-synaptically connected to motor circuits.•Most manipulations of emotion-related structures impact motor behavior.•Neural networks for emotional modulation of movement include limbic system and motor-related regions•Studying emotion-motor circuit connectivity in animals offers insights into human physiopathology.</description><subject>Animals</subject><subject>Basal ganglia</subject><subject>Brain</subject><subject>Brain - physiology</subject><subject>Emotional states</subject><subject>Emotions - physiology</subject><subject>Humans</subject><subject>Life Sciences</subject><subject>Limbic system</subject><subject>Motor behavior</subject><subject>Motor system</subject><subject>Movement</subject><subject>Movement - physiology</subject><subject>Neuromodulators</subject><subject>Neuronal circuits</subject><subject>Neurons</subject><subject>Neurons and Cognition</subject><subject>Psychology and behavior</subject><subject>Sensory-motor control</subject><issn>0149-7634</issn><issn>1873-7528</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkE1LxDAQhoMoun78Be1RD13z2STeFlk_YMGL4jGkyRSzbBtN2gX_vV2qe_U0My_PzMCD0BXBc4JJdbuedzDUISbYzimmbEwFl-IAzYiSrJSCqkM0w4TrUlaMn6DTnNcYY4qZOEYnTGpdYS5niC_b2IfYFaErrNt1d8X7B3QFTHkuWoC-GIeYCheSG0Kfz9FRYzcZLn7rGXp7WL7eP5Wrl8fn-8WqdLyq-lJhrrwW4Jh2SsqaeAzUuRqY9bTRlKumdp5b57wQAmrmOafWilpzrAlr2Bm6me5-2I35TKG16dtEG8zTYmV2GeaMEEXIlozs9cR-pvg1QO5NG7KDzcZ2EIdsqNJMsYpyOaJyQl2KOSdo9rcJNju9Zm32es1Or5n0jpuXv0-GugW_3_vzOQKLCYBRyzZAMtkF6Bz4kMD1xsfw75Mf4vCPBg</recordid><startdate>20231201</startdate><enddate>20231201</enddate><creator>Braine, Anaelle</creator><creator>Georges, François</creator><general>Elsevier Ltd</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-2628-2638</orcidid></search><sort><creationdate>20231201</creationdate><title>Emotion in action: When emotions meet motor circuits</title><author>Braine, Anaelle ; Georges, François</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c466t-8048d95ec39c877b1d0e2ccbe3ad2f9248fbcd4accd555eb3d442aa5b940913f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Basal ganglia</topic><topic>Brain</topic><topic>Brain - physiology</topic><topic>Emotional states</topic><topic>Emotions - physiology</topic><topic>Humans</topic><topic>Life Sciences</topic><topic>Limbic system</topic><topic>Motor behavior</topic><topic>Motor system</topic><topic>Movement</topic><topic>Movement - physiology</topic><topic>Neuromodulators</topic><topic>Neuronal circuits</topic><topic>Neurons</topic><topic>Neurons and Cognition</topic><topic>Psychology and behavior</topic><topic>Sensory-motor control</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Braine, Anaelle</creatorcontrib><creatorcontrib>Georges, François</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Neuroscience and biobehavioral reviews</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Braine, Anaelle</au><au>Georges, François</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Emotion in action: When emotions meet motor circuits</atitle><jtitle>Neuroscience and biobehavioral reviews</jtitle><addtitle>Neurosci Biobehav Rev</addtitle><date>2023-12-01</date><risdate>2023</risdate><volume>155</volume><spage>105475</spage><epage>105475</epage><pages>105475-105475</pages><artnum>105475</artnum><issn>0149-7634</issn><eissn>1873-7528</eissn><abstract>The brain is a remarkably complex organ responsible for a wide range of functions, including the modulation of emotional states and movement. Neuronal circuits are believed to play a crucial role in integrating sensory, cognitive, and emotional information to ultimately guide motor behavior. Over the years, numerous studies employing diverse techniques such as electrophysiology, imaging, and optogenetics have revealed a complex network of neural circuits involved in the regulation of emotional or motor processes. Emotions can exert a substantial influence on motor performance, encompassing both everyday activities and pathological conditions. The aim of this review is to explore how emotional states can shape movements by connecting the neural circuits for emotional processing to motor neural circuits. We first provide a comprehensive overview of the impact of different emotional states on motor control in humans and rodents. In line with behavioral studies, we set out to identify emotion-related structures capable of modulating motor output, behaviorally and anatomically. Neuronal circuits involved in emotional processing are extensively connected to the motor system. These circuits can drive emotional behavior, essential for survival, but can also continuously shape ongoing movement. In summary, the investigation of the intricate relationship between emotion and movement offers valuable insights into human behavior, including opportunities to enhance performance, and holds promise for improving mental and physical health. This review integrates findings from multiple scientific approaches, including anatomical tracing, circuit-based dissection, and behavioral studies, conducted in both animal and human subjects. By incorporating these different methodologies, we aim to present a comprehensive overview of the current understanding of the emotional modulation of movement in both physiological and pathological conditions.
•Emotions significantly influence motor performance in daily activities and pathological conditions.•Numerous emotion-related structures are mono-synaptically connected to motor circuits.•Most manipulations of emotion-related structures impact motor behavior.•Neural networks for emotional modulation of movement include limbic system and motor-related regions•Studying emotion-motor circuit connectivity in animals offers insights into human physiopathology.</abstract><cop>United States</cop><pub>Elsevier Ltd</pub><pmid>37996047</pmid><doi>10.1016/j.neubiorev.2023.105475</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-2628-2638</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Basal ganglia Brain Brain - physiology Emotional states Emotions - physiology Humans Life Sciences Limbic system Motor behavior Motor system Movement Movement - physiology Neuromodulators Neuronal circuits Neurons Neurons and Cognition Psychology and behavior Sensory-motor control |
title | Emotion in action: When emotions meet motor circuits |
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