Neural Responses to Heartbeats in the Default Network Encode the Self in Spontaneous Thoughts
The default network (DN) has been consistently associated with self-related cognition, but also to bodily state monitoring and autonomic regulation. We hypothesized that these two seemingly disparate functional roles of the DN are functionally coupled, in line with theories proposing that selfhood i...
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description | The default network (DN) has been consistently associated with self-related cognition, but also to bodily state monitoring and autonomic regulation. We hypothesized that these two seemingly disparate functional roles of the DN are functionally coupled, in line with theories proposing that selfhood is grounded in the neural monitoring of internal organs, such as the heart. We measured with magnetoencephalograhy neural responses evoked by heartbeats while human participants freely mind-wandered. When interrupted by a visual stimulus at random intervals, participants scored the self-relatedness of the interrupted thought. They evaluated their involvement as the first-person perspective subject or agent in the thought ("I"), and on another scale to what degree they were thinking about themselves ("Me"). During the interrupted thought, neural responses to heartbeats in two regions of the DN, the ventral precuneus and the ventromedial prefrontal cortex, covaried, respectively, with the "I" and the "Me" dimensions of the self, even at the single-trial level. No covariation between self-relatedness and peripheral autonomic measures (heart rate, heart rate variability, pupil diameter, electrodermal activity, respiration rate, and phase) or alpha power was observed. Our results reveal a direct link between selfhood and neural responses to heartbeats in the DN and thus directly support theories grounding selfhood in the neural monitoring of visceral inputs. More generally, the tight functional coupling between self-related processing and cardiac monitoring observed here implies that, even in the absence of measured changes in peripheral bodily measures, physiological and cognitive functions have to be considered jointly in the DN.
The default network (DN) has been consistently associated with self-processing but also with autonomic regulation. We hypothesized that these two functions could be functionally coupled in the DN, inspired by theories according to which selfhood is grounded in the neural monitoring of internal organs. Using magnetoencephalography, we show that heartbeat-evoked responses (HERs) in the DN covary with the self-relatedness of ongoing spontaneous thoughts. HER amplitude in the ventral precuneus covaried with the "I" self-dimension, whereas HER amplitude in the ventromedial prefrontal cortex encoded the "Me" self-dimension. Our experimental results directly support theories rooting selfhood in the neural monitoring of internal organs. We propose |
doi_str_mv | 10.1523/JNEUROSCI.0262-16.2016 |
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The default network (DN) has been consistently associated with self-processing but also with autonomic regulation. We hypothesized that these two functions could be functionally coupled in the DN, inspired by theories according to which selfhood is grounded in the neural monitoring of internal organs. Using magnetoencephalography, we show that heartbeat-evoked responses (HERs) in the DN covary with the self-relatedness of ongoing spontaneous thoughts. HER amplitude in the ventral precuneus covaried with the "I" self-dimension, whereas HER amplitude in the ventromedial prefrontal cortex encoded the "Me" self-dimension. Our experimental results directly support theories rooting selfhood in the neural monitoring of internal organs. We propose a novel functional framework for the DN, where self-processing is coupled with physiological monitoring.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.0262-16.2016</identifier><identifier>PMID: 27466329</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Adult ; Attention - physiology ; Autonomic Nervous System - physiology ; Cognition - physiology ; Feedback, Physiological - physiology ; Female ; Heart Rate - physiology ; Humans ; Male ; Nerve Net - physiology ; Prefrontal Cortex - physiology ; Thinking - physiology</subject><ispartof>The Journal of neuroscience, 2016-07, Vol.36 (30), p.7829-7840</ispartof><rights>Copyright © 2016 Babo-Rebelo et al.</rights><rights>Copyright © 2016 Babo-Rebelo et al. 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c566t-912394695406309dc899d824fe1d9b4bc78c0ad991b672a2c4a30ce36ccf5d3b3</citedby><orcidid>0000-0001-8664-7427 ; 0000-0002-6839-7994 ; 0000-0001-8480-5831</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4961773/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4961773/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27922,27923,53789,53791</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27466329$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Babo-Rebelo, Mariana</creatorcontrib><creatorcontrib>Richter, Craig G</creatorcontrib><creatorcontrib>Tallon-Baudry, Catherine</creatorcontrib><title>Neural Responses to Heartbeats in the Default Network Encode the Self in Spontaneous Thoughts</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>The default network (DN) has been consistently associated with self-related cognition, but also to bodily state monitoring and autonomic regulation. We hypothesized that these two seemingly disparate functional roles of the DN are functionally coupled, in line with theories proposing that selfhood is grounded in the neural monitoring of internal organs, such as the heart. We measured with magnetoencephalograhy neural responses evoked by heartbeats while human participants freely mind-wandered. When interrupted by a visual stimulus at random intervals, participants scored the self-relatedness of the interrupted thought. They evaluated their involvement as the first-person perspective subject or agent in the thought ("I"), and on another scale to what degree they were thinking about themselves ("Me"). During the interrupted thought, neural responses to heartbeats in two regions of the DN, the ventral precuneus and the ventromedial prefrontal cortex, covaried, respectively, with the "I" and the "Me" dimensions of the self, even at the single-trial level. No covariation between self-relatedness and peripheral autonomic measures (heart rate, heart rate variability, pupil diameter, electrodermal activity, respiration rate, and phase) or alpha power was observed. Our results reveal a direct link between selfhood and neural responses to heartbeats in the DN and thus directly support theories grounding selfhood in the neural monitoring of visceral inputs. More generally, the tight functional coupling between self-related processing and cardiac monitoring observed here implies that, even in the absence of measured changes in peripheral bodily measures, physiological and cognitive functions have to be considered jointly in the DN.
The default network (DN) has been consistently associated with self-processing but also with autonomic regulation. We hypothesized that these two functions could be functionally coupled in the DN, inspired by theories according to which selfhood is grounded in the neural monitoring of internal organs. Using magnetoencephalography, we show that heartbeat-evoked responses (HERs) in the DN covary with the self-relatedness of ongoing spontaneous thoughts. HER amplitude in the ventral precuneus covaried with the "I" self-dimension, whereas HER amplitude in the ventromedial prefrontal cortex encoded the "Me" self-dimension. Our experimental results directly support theories rooting selfhood in the neural monitoring of internal organs. We propose a novel functional framework for the DN, where self-processing is coupled with physiological monitoring.</description><subject>Adult</subject><subject>Attention - physiology</subject><subject>Autonomic Nervous System - physiology</subject><subject>Cognition - physiology</subject><subject>Feedback, Physiological - physiology</subject><subject>Female</subject><subject>Heart Rate - physiology</subject><subject>Humans</subject><subject>Male</subject><subject>Nerve Net - physiology</subject><subject>Prefrontal Cortex - physiology</subject><subject>Thinking - physiology</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkctOGzEUhi1UBCH0FZCX3Uw4vsQebypVaQpUKEgJLCvL4zlDpp2M07GniLdn0tCo7FidxX_R-fURcsFgwqZcXH5fzB-Wd6vZzQS44hlTEw5MHZHRoJqMS2AfyAi4hkxJLU_JWYw_AUAD0yfklGuplOBmRH4ssO9cQ5cYt6GNGGkK9Bpdlwp0KdK6pWmN9CtWrm8SXWB6Ct0vOm99KPGvtMKm2tlWQz65FkMf6f069I_rFM_JceWaiB9f75g8fJvfz66z27urm9mX28xPlUqZYVwYqcxUghJgSp8bU-ZcVshKU8jC69yDK41hhdLccS-dAI9CeV9NS1GIMfm87932xQZLj20aRtltV29c92yDq-1bpa3X9jH8sdIoprUYCj69FnThd48x2U0dPTbNfpBlOWO5VobDO6ygh_-5lINV7a2-CzF2WB0-YmB3GO0Bo91htEzZHcYhePH_nkPsHzfxAiVvmuc</recordid><startdate>20160727</startdate><enddate>20160727</enddate><creator>Babo-Rebelo, Mariana</creator><creator>Richter, Craig G</creator><creator>Tallon-Baudry, Catherine</creator><general>Society for Neuroscience</general><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>7TK</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8664-7427</orcidid><orcidid>https://orcid.org/0000-0002-6839-7994</orcidid><orcidid>https://orcid.org/0000-0001-8480-5831</orcidid></search><sort><creationdate>20160727</creationdate><title>Neural Responses to Heartbeats in the Default Network Encode the Self in Spontaneous Thoughts</title><author>Babo-Rebelo, Mariana ; Richter, Craig G ; Tallon-Baudry, Catherine</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c566t-912394695406309dc899d824fe1d9b4bc78c0ad991b672a2c4a30ce36ccf5d3b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adult</topic><topic>Attention - physiology</topic><topic>Autonomic Nervous System - physiology</topic><topic>Cognition - physiology</topic><topic>Feedback, Physiological - physiology</topic><topic>Female</topic><topic>Heart Rate - physiology</topic><topic>Humans</topic><topic>Male</topic><topic>Nerve Net - physiology</topic><topic>Prefrontal Cortex - physiology</topic><topic>Thinking - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Babo-Rebelo, Mariana</creatorcontrib><creatorcontrib>Richter, Craig G</creatorcontrib><creatorcontrib>Tallon-Baudry, Catherine</creatorcontrib><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>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Babo-Rebelo, Mariana</au><au>Richter, Craig G</au><au>Tallon-Baudry, Catherine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural Responses to Heartbeats in the Default Network Encode the Self in Spontaneous Thoughts</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2016-07-27</date><risdate>2016</risdate><volume>36</volume><issue>30</issue><spage>7829</spage><epage>7840</epage><pages>7829-7840</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>The default network (DN) has been consistently associated with self-related cognition, but also to bodily state monitoring and autonomic regulation. We hypothesized that these two seemingly disparate functional roles of the DN are functionally coupled, in line with theories proposing that selfhood is grounded in the neural monitoring of internal organs, such as the heart. We measured with magnetoencephalograhy neural responses evoked by heartbeats while human participants freely mind-wandered. When interrupted by a visual stimulus at random intervals, participants scored the self-relatedness of the interrupted thought. They evaluated their involvement as the first-person perspective subject or agent in the thought ("I"), and on another scale to what degree they were thinking about themselves ("Me"). During the interrupted thought, neural responses to heartbeats in two regions of the DN, the ventral precuneus and the ventromedial prefrontal cortex, covaried, respectively, with the "I" and the "Me" dimensions of the self, even at the single-trial level. No covariation between self-relatedness and peripheral autonomic measures (heart rate, heart rate variability, pupil diameter, electrodermal activity, respiration rate, and phase) or alpha power was observed. Our results reveal a direct link between selfhood and neural responses to heartbeats in the DN and thus directly support theories grounding selfhood in the neural monitoring of visceral inputs. More generally, the tight functional coupling between self-related processing and cardiac monitoring observed here implies that, even in the absence of measured changes in peripheral bodily measures, physiological and cognitive functions have to be considered jointly in the DN.
The default network (DN) has been consistently associated with self-processing but also with autonomic regulation. We hypothesized that these two functions could be functionally coupled in the DN, inspired by theories according to which selfhood is grounded in the neural monitoring of internal organs. Using magnetoencephalography, we show that heartbeat-evoked responses (HERs) in the DN covary with the self-relatedness of ongoing spontaneous thoughts. HER amplitude in the ventral precuneus covaried with the "I" self-dimension, whereas HER amplitude in the ventromedial prefrontal cortex encoded the "Me" self-dimension. Our experimental results directly support theories rooting selfhood in the neural monitoring of internal organs. We propose a novel functional framework for the DN, where self-processing is coupled with physiological monitoring.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>27466329</pmid><doi>10.1523/JNEUROSCI.0262-16.2016</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-8664-7427</orcidid><orcidid>https://orcid.org/0000-0002-6839-7994</orcidid><orcidid>https://orcid.org/0000-0001-8480-5831</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Attention - physiology Autonomic Nervous System - physiology Cognition - physiology Feedback, Physiological - physiology Female Heart Rate - physiology Humans Male Nerve Net - physiology Prefrontal Cortex - physiology Thinking - physiology |
title | Neural Responses to Heartbeats in the Default Network Encode the Self in Spontaneous Thoughts |
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