Neural Responses to Heartbeats in the Default Network Encode the Self in Spontaneous Thoughts

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 firstperson 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. Key words: default network; heartbeat-evoked responses; MEG; self; spontaneous cognition IntroductionThe default network (DN) has been consistently associated with self-related processing in fMRI studies (Buckner et al., 2008; Qin and Northoff, 2011;Andrews-Hanna et al., 2014). However, the DN is also involved in central autonomic processing (Thayer et al., 2012;Beissner et al., 2013) and includes prefrontal visceral cingulate areas (Vogt and Derbyshire, 2009), which respond to heartbeats (Park et al., 2014) and modulate heart rate when stimulated (Van Eden and Buijs, 2000). This colocalization between a Received Jan. 25, 2016; revised April 14, 2016; accepted May 19, 2016. Author The authors declare no competing financial interests. This article is freely available online through the J Neurosci Author Open Choice option. Significance StatementThe 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. ...

Affective interoceptive inference: Evidence from heart‐beat evoked brain potentials

“…First, we did not control for other cardio-respiratory parameters that might affect the HEP amplitude changes (Babo-Rebelo et al, 2016;Park, Correia, Ducorps, & Tallon-Baudry, 2014), and therefore, we are unable to account for their potential impact in our findings. First, we did not control for other cardio-respiratory parameters that might affect the HEP amplitude changes (Babo-Rebelo et al, 2016;Park, Correia, Ducorps, & Tallon-Baudry, 2014), and therefore, we are unable to account for their potential impact in our findings.…”

“…Our study has a number of limitations that are worth noting. First, we did not control for other cardio-respiratory parameters that might affect the HEP amplitude changes (Babo-Rebelo et al, 2016;Park, Correia, Ducorps, & Tallon-Baudry, 2014), and therefore, we are unable to account for their potential impact in our findings. Similarly, the short intertrial interval of our experimental setup does not allow the computation of cardiac parameters, such as the interbeat interval and activity in the heart period power spectrum (Rajendra Acharya, Paul Joseph, Kannathal, Lim, & Suri, 2006).…”

“…In brief, data were submitted to a repeated measures, two-tailed cluster mass permutation test (Bullmore et al, 1999) using a family-wise alpha level of 0.05 (i.e., 5,226 total comparisons). Where appropriate, we calculated Bayesian statistics for null effects (Babo-Rebelo et al, 2016;Park et al, 2017;Rouder, Speckman, Sun, Morey, & Iverson, 2009;Salomon et al, 2016) using the online Bayes factor calculation tool (http://pcl. Repeated measures t tests were performed for each comparison using the original data and 2,500 random within-participant permutations of the data.…”

“…To further ensure that the HEP changes that we observe are not influenced by CFA artifacts, and they are truly locked to the participants' heartbeat, we created surrogated R-peaks by shifting the onset of the original R-peak (e.g., Babo-Rebelo, Richter, & Tallon-Baudry, 2016;Park et al, 2017). R-peaks were shifted within a time window of −500 to +500 ms and they were shifted by the same amount separately for each subject and each of the eight conditions.…”

Respiration competes with theta for modulating parietal cortex neurons

“…Interestingly, recent studies are starting to unveil relationships between oscillatory activity produced by different organ systems. For instance, Tallon-Baudry and collaborators have shown that ascending signals from the heart and gastrointestinal tract modulate brain dynamics and affect perception, emotion and cognition [10][11][12][13]. In particular, the EEG alpha rhythm was shown to be modulated by the phase of the gastric cycle [7].…”