Single neurons in the thalamus and subthalamic nucleus process cardiac and respiratory signals in humans
Visceral signals are constantly processed by our central nervous system, enable homeostatic regulation, and influence perception, emotion, and cognition. While visceral processes at the cortical level have been extensively studied using non-invasive imaging techniques, very few studies have investig...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2024-03, Vol.121 (11), p.e2316365121 |
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creator | De Falco, Emanuela Solcà, Marco Bernasconi, Fosco Babo-Rebelo, Mariana Young, Nicole Sammartino, Francesco Tallon-Baudry, Catherine Navarro, Vincent Rezai, Ali R Krishna, Vibhor Blanke, Olaf |
description | Visceral signals are constantly processed by our central nervous system, enable homeostatic regulation, and influence perception, emotion, and cognition. While visceral processes at the cortical level have been extensively studied using non-invasive imaging techniques, very few studies have investigated how this information is processed at the single neuron level, both in humans and animals. Subcortical regions, relaying signals from peripheral interoceptors to cortical structures, are particularly understudied and how visceral information is processed in thalamic and subthalamic structures remains largely unknown. Here, we took advantage of intraoperative microelectrode recordings in patients undergoing surgery for deep brain stimulation (DBS) to investigate the activity of single neurons related to cardiac and respiratory functions in three subcortical regions: ventral intermedius nucleus (Vim) and ventral caudalis nucleus (Vc) of the thalamus, and subthalamic nucleus (STN). We report that the activity of a large portion of the recorded neurons (about 70%) was modulated by either the heartbeat, the cardiac inter-beat interval, or the respiration. These cardiac and respiratory response patterns varied largely across neurons both in terms of timing and their kind of modulation. A substantial proportion of these visceral neurons (30%) was responsive to more than one of the tested signals, underlining specialization and integration of cardiac and respiratory signals in STN and thalamic neurons. By extensively describing single unit activity related to cardiorespiratory function in thalamic and subthalamic neurons, our results highlight the major role of these subcortical regions in the processing of visceral signals. |
doi_str_mv | 10.1073/pnas.2316365121 |
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While visceral processes at the cortical level have been extensively studied using non-invasive imaging techniques, very few studies have investigated how this information is processed at the single neuron level, both in humans and animals. Subcortical regions, relaying signals from peripheral interoceptors to cortical structures, are particularly understudied and how visceral information is processed in thalamic and subthalamic structures remains largely unknown. Here, we took advantage of intraoperative microelectrode recordings in patients undergoing surgery for deep brain stimulation (DBS) to investigate the activity of single neurons related to cardiac and respiratory functions in three subcortical regions: ventral intermedius nucleus (Vim) and ventral caudalis nucleus (Vc) of the thalamus, and subthalamic nucleus (STN). We report that the activity of a large portion of the recorded neurons (about 70%) was modulated by either the heartbeat, the cardiac inter-beat interval, or the respiration. These cardiac and respiratory response patterns varied largely across neurons both in terms of timing and their kind of modulation. A substantial proportion of these visceral neurons (30%) was responsive to more than one of the tested signals, underlining specialization and integration of cardiac and respiratory signals in STN and thalamic neurons. By extensively describing single unit activity related to cardiorespiratory function in thalamic and subthalamic neurons, our results highlight the major role of these subcortical regions in the processing of visceral signals.</description><identifier>ISSN: 0027-8424</identifier><identifier>ISSN: 1091-6490</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2316365121</identifier><identifier>PMID: 38451949</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Central nervous system ; Cognition ; Deep Brain Stimulation ; Electrical stimuli ; Heart ; Humans ; Imaging techniques ; Information processing ; Life Sciences ; Microelectrodes ; Neuroimaging ; Neurons ; Neurons - physiology ; Respiration ; Signal processing ; Solitary tract nucleus ; Subthalamic Nucleus ; Thalamus ; Thalamus - physiology ; Unit activity</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2024-03, Vol.121 (11), p.e2316365121</ispartof><rights>Copyright National Academy of Sciences Mar 12, 2024</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><citedby>FETCH-LOGICAL-c400t-65290eba82f22e053e95c8ccb953b575cde7cd48e115e6899f3e4b0103b5cbc03</citedby><cites>FETCH-LOGICAL-c400t-65290eba82f22e053e95c8ccb953b575cde7cd48e115e6899f3e4b0103b5cbc03</cites><orcidid>0000-0002-9745-3983 ; 0000-0003-0422-5867 ; 0000-0002-4141-4192 ; 0000-0001-8664-7427 ; 0000-0001-8480-5831 ; 0000-0002-2275-7229</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38451949$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04790151$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>De Falco, Emanuela</creatorcontrib><creatorcontrib>Solcà, Marco</creatorcontrib><creatorcontrib>Bernasconi, Fosco</creatorcontrib><creatorcontrib>Babo-Rebelo, Mariana</creatorcontrib><creatorcontrib>Young, Nicole</creatorcontrib><creatorcontrib>Sammartino, Francesco</creatorcontrib><creatorcontrib>Tallon-Baudry, Catherine</creatorcontrib><creatorcontrib>Navarro, Vincent</creatorcontrib><creatorcontrib>Rezai, Ali R</creatorcontrib><creatorcontrib>Krishna, Vibhor</creatorcontrib><creatorcontrib>Blanke, Olaf</creatorcontrib><title>Single neurons in the thalamus and subthalamic nucleus process cardiac and respiratory signals in humans</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Visceral signals are constantly processed by our central nervous system, enable homeostatic regulation, and influence perception, emotion, and cognition. While visceral processes at the cortical level have been extensively studied using non-invasive imaging techniques, very few studies have investigated how this information is processed at the single neuron level, both in humans and animals. Subcortical regions, relaying signals from peripheral interoceptors to cortical structures, are particularly understudied and how visceral information is processed in thalamic and subthalamic structures remains largely unknown. Here, we took advantage of intraoperative microelectrode recordings in patients undergoing surgery for deep brain stimulation (DBS) to investigate the activity of single neurons related to cardiac and respiratory functions in three subcortical regions: ventral intermedius nucleus (Vim) and ventral caudalis nucleus (Vc) of the thalamus, and subthalamic nucleus (STN). We report that the activity of a large portion of the recorded neurons (about 70%) was modulated by either the heartbeat, the cardiac inter-beat interval, or the respiration. These cardiac and respiratory response patterns varied largely across neurons both in terms of timing and their kind of modulation. A substantial proportion of these visceral neurons (30%) was responsive to more than one of the tested signals, underlining specialization and integration of cardiac and respiratory signals in STN and thalamic neurons. 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While visceral processes at the cortical level have been extensively studied using non-invasive imaging techniques, very few studies have investigated how this information is processed at the single neuron level, both in humans and animals. Subcortical regions, relaying signals from peripheral interoceptors to cortical structures, are particularly understudied and how visceral information is processed in thalamic and subthalamic structures remains largely unknown. Here, we took advantage of intraoperative microelectrode recordings in patients undergoing surgery for deep brain stimulation (DBS) to investigate the activity of single neurons related to cardiac and respiratory functions in three subcortical regions: ventral intermedius nucleus (Vim) and ventral caudalis nucleus (Vc) of the thalamus, and subthalamic nucleus (STN). We report that the activity of a large portion of the recorded neurons (about 70%) was modulated by either the heartbeat, the cardiac inter-beat interval, or the respiration. These cardiac and respiratory response patterns varied largely across neurons both in terms of timing and their kind of modulation. A substantial proportion of these visceral neurons (30%) was responsive to more than one of the tested signals, underlining specialization and integration of cardiac and respiratory signals in STN and thalamic neurons. 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subjects | Animals Central nervous system Cognition Deep Brain Stimulation Electrical stimuli Heart Humans Imaging techniques Information processing Life Sciences Microelectrodes Neuroimaging Neurons Neurons - physiology Respiration Signal processing Solitary tract nucleus Subthalamic Nucleus Thalamus Thalamus - physiology Unit activity |
title | Single neurons in the thalamus and subthalamic nucleus process cardiac and respiratory signals in humans |
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