David Braun, Lotus Shareef-Trudeau, Swetha Rao, Christine Chesebrough, Julia W Y Kam, Aaron Kucyi
{"title":"神经对心跳的敏感性是由自发思考过程中情感唤起的波动所调节的。","authors":"David Braun, Lotus Shareef-Trudeau, Swetha Rao, Christine Chesebrough, Julia W Y Kam, Aaron Kucyi","doi":"10.1523/JNEUROSCI.0608-25.2025","DOIUrl":null,"url":null,"abstract":"<p><p>Spontaneous thoughts, occupying much of one's awake time in daily life, are often colored by emotional qualities. While spontaneous thoughts have been associated with various neural correlates, the relationship between subjective qualities of ongoing experiences and the brain's sensitivity to bodily signals (i.e., interoception) remains largely unexplored. Given the well-established role of interoception in emotion, clarifying this relationship may elucidate how processes relevant to mental health, such as arousal and anxiety, are regulated. We used EEG and ECG to measure the heartbeat evoked potential (HEP), an index of interoceptive processing, while 51 adult participants (34 male, 20 female) visually fixated on a cross image and let their minds wander freely. At pseudo-random intervals, participants reported their momentary level of arousal. This measure of affective arousal was highly variable within and between individuals but was statistically unrelated to several markers of physiological arousal, including heart rate, heart rate variability, time on task, and EEG alpha power at posterior electrodes. A cluster-based permutation analysis revealed that the HEP amplitude was increased during low relative to high affective arousal in a set of frontal electrodes during the 340 - 356 millisecond window after heartbeat onset. This HEP effect was more pronounced in individuals who reported high, relative to low, levels of trait anxiety. Together, our results offer novel evidence that at varying levels of trait anxiety, the brain differentially modulates sensitivity to bodily signals in coordination with the momentary, spontaneous experience of affective arousal-a mechanism that may operate independently of physiological arousal.<b>Significance Statement</b> Our findings highlight the relationships between spontaneous fluctuations in affective arousal, brain-body interactions, and anxiety, offering new insights into how interoception fluctuates with changes in internal states. By showing that interoceptive processing is heightened during lower affective arousal and that this effect is amplified in individuals with higher trait anxiety, our study suggests the brain adaptively downregulates interoceptive sensitivity in response to fluctuating internal states. These results have implications for understanding how spontaneous thoughts shape interoception and emotion, particularly in clinical contexts where dysregulated interoception is linked to anxiety and mood disorders. More broadly, our work underscores the need to distinguish between different forms of arousal, advancing understanding of the taxonomy and ways of measuring arousal.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0000,"publicationDate":"2025-10-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Neural sensitivity to the heartbeat is modulated by fluctuations in affective arousal during spontaneous thought.\",\"authors\":\"David Braun, Lotus Shareef-Trudeau, Swetha Rao, Christine Chesebrough, Julia W Y Kam, Aaron Kucyi\",\"doi\":\"10.1523/JNEUROSCI.0608-25.2025\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Spontaneous thoughts, occupying much of one's awake time in daily life, are often colored by emotional qualities. While spontaneous thoughts have been associated with various neural correlates, the relationship between subjective qualities of ongoing experiences and the brain's sensitivity to bodily signals (i.e., interoception) remains largely unexplored. Given the well-established role of interoception in emotion, clarifying this relationship may elucidate how processes relevant to mental health, such as arousal and anxiety, are regulated. We used EEG and ECG to measure the heartbeat evoked potential (HEP), an index of interoceptive processing, while 51 adult participants (34 male, 20 female) visually fixated on a cross image and let their minds wander freely. At pseudo-random intervals, participants reported their momentary level of arousal. This measure of affective arousal was highly variable within and between individuals but was statistically unrelated to several markers of physiological arousal, including heart rate, heart rate variability, time on task, and EEG alpha power at posterior electrodes. A cluster-based permutation analysis revealed that the HEP amplitude was increased during low relative to high affective arousal in a set of frontal electrodes during the 340 - 356 millisecond window after heartbeat onset. This HEP effect was more pronounced in individuals who reported high, relative to low, levels of trait anxiety. Together, our results offer novel evidence that at varying levels of trait anxiety, the brain differentially modulates sensitivity to bodily signals in coordination with the momentary, spontaneous experience of affective arousal-a mechanism that may operate independently of physiological arousal.<b>Significance Statement</b> Our findings highlight the relationships between spontaneous fluctuations in affective arousal, brain-body interactions, and anxiety, offering new insights into how interoception fluctuates with changes in internal states. By showing that interoceptive processing is heightened during lower affective arousal and that this effect is amplified in individuals with higher trait anxiety, our study suggests the brain adaptively downregulates interoceptive sensitivity in response to fluctuating internal states. These results have implications for understanding how spontaneous thoughts shape interoception and emotion, particularly in clinical contexts where dysregulated interoception is linked to anxiety and mood disorders. More broadly, our work underscores the need to distinguish between different forms of arousal, advancing understanding of the taxonomy and ways of measuring arousal.</p>\",\"PeriodicalId\":50114,\"journal\":{\"name\":\"Journal of Neuroscience\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":4.0000,\"publicationDate\":\"2025-10-02\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of Neuroscience\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1523/JNEUROSCI.0608-25.2025\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.0608-25.2025","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
Neural sensitivity to the heartbeat is modulated by fluctuations in affective arousal during spontaneous thought.
Spontaneous thoughts, occupying much of one's awake time in daily life, are often colored by emotional qualities. While spontaneous thoughts have been associated with various neural correlates, the relationship between subjective qualities of ongoing experiences and the brain's sensitivity to bodily signals (i.e., interoception) remains largely unexplored. Given the well-established role of interoception in emotion, clarifying this relationship may elucidate how processes relevant to mental health, such as arousal and anxiety, are regulated. We used EEG and ECG to measure the heartbeat evoked potential (HEP), an index of interoceptive processing, while 51 adult participants (34 male, 20 female) visually fixated on a cross image and let their minds wander freely. At pseudo-random intervals, participants reported their momentary level of arousal. This measure of affective arousal was highly variable within and between individuals but was statistically unrelated to several markers of physiological arousal, including heart rate, heart rate variability, time on task, and EEG alpha power at posterior electrodes. A cluster-based permutation analysis revealed that the HEP amplitude was increased during low relative to high affective arousal in a set of frontal electrodes during the 340 - 356 millisecond window after heartbeat onset. This HEP effect was more pronounced in individuals who reported high, relative to low, levels of trait anxiety. Together, our results offer novel evidence that at varying levels of trait anxiety, the brain differentially modulates sensitivity to bodily signals in coordination with the momentary, spontaneous experience of affective arousal-a mechanism that may operate independently of physiological arousal.Significance Statement Our findings highlight the relationships between spontaneous fluctuations in affective arousal, brain-body interactions, and anxiety, offering new insights into how interoception fluctuates with changes in internal states. By showing that interoceptive processing is heightened during lower affective arousal and that this effect is amplified in individuals with higher trait anxiety, our study suggests the brain adaptively downregulates interoceptive sensitivity in response to fluctuating internal states. These results have implications for understanding how spontaneous thoughts shape interoception and emotion, particularly in clinical contexts where dysregulated interoception is linked to anxiety and mood disorders. More broadly, our work underscores the need to distinguish between different forms of arousal, advancing understanding of the taxonomy and ways of measuring arousal.
期刊介绍:
JNeurosci (ISSN 0270-6474) is an official journal of the Society for Neuroscience. It is published weekly by the Society, fifty weeks a year, one volume a year. JNeurosci publishes papers on a broad range of topics of general interest to those working on the nervous system. Authors now have an Open Choice option for their published articles