Is the cardiac monitoring function related to the self in both the default network and right anterior insula?

Abstract

The self has been proposed to be rooted in the neural monitoring of internal bodily signals and might thus involve interoceptive areas, notably the right anterior insula (rAI). However, studies on the self consistently showed the involvement of midline default network (DN) nodes, without referring to visceral monitoring. Here, we investigate this apparent discrepancy. We previously showed that neural responses to heartbeats in the DN encode two different self-dimensions, the agentive 'I' and the introspective 'Me', in a whole-brain analysis of magnetoencephalography (MEG) data. Here, we confirm and anatomically refine this result with intracranial recordings (intracranial electroencephalography, iEEG). In two patients, we show a parametric modulation of neural responses to heartbeats by the self-relatedness of thoughts, at the single trial level. A region-of-interest analysis of the insula reveals that MEG responses to heartbeats in the rAI encode the 'I' self-dimension. The effect in rAI was weaker than in the DN and was replicated in iEEG data in one patient out of two. We propose that a common mechanism, the neural monitoring of cardiac signals, underlies the self in both the DN and rAI. This might reconcile studies on the self highlighting the DN, with studies on interoception focusing on the insula.This article is part of the themed issue 'Interoception beyond homeostasis: affect, cognition and mental health'.

Keywords: heartbeat-evoked responses; interoception; intracranial electroencephalography; magnetoencephalography; neural responses to heartbeats; spontaneous cognition.

Figure 1.

Experimental paradigm. (a) Time course of a trial. Each trial consisted of a fixation period interrupted by a visual stimulus. During fixation, participants were asked to let their thoughts develop freely. Participants pressed a button in response to the visual stimulus and had to remember the thought that was interrupted by the visual stimulus. They rated this thought along four scales (‘I’, ‘Me’, Time and Valence) or could skip the ratings if the interrupted thought was unclear or if they were not sure how to use the scales. (b) Intracranial electroencephalographic (iEEG) and magnetoencephalographic (MEG) data were locked to the two R-peaks of the electrocardiogram (ECG) preceding the visual stimulus, to compute HERs during the thought. (c) Examples of thoughts along the two scales of self-relatedness. The ‘I’ scale described the engagement of the participant as the protagonist or the agent in the thought. The ‘Me’ scale described the content of the thought, that can be oriented either toward oneself or toward an external object, event or person (adapted from [25]).

Figure 2.

Overlap between DN, self and autonomic regulation meta-analyses. The orange outline represents the DN, as defined in Laird [35]. Green outlines highlight regions responsible for sympathetic (dark green) and parasympathetic (light green) regulation [34]. The results of the automated [31] meta-analysis on the term ‘self’ are presented in yellow (reverse inference map) and in blue (forward inference map). The sagittal view (left) shows that the reverse inference map of the self is associated with the DN, where it overlaps with autonomic regulation regions. The axial view (right) shows that the rAI is associated with the forward inference map of the self and overlaps with autonomic regulation regions.

Figure 3.

The trial-by-trial amplitude of HERs in the vmPFC correlates with the involvement of the ‘Me’ in spontaneous thoughts (patient 1). (a) Time course of the Pearson correlation coefficient r between the trial-by-trial HER amplitude and the ratings on the ‘Me’ scale (black), and HERs (±s.e.m.) for ‘high’ (dark red) and ‘low’ (light pink) ratings on the ‘Me’ scale (median split of ratings), for recording site 2 (circled dot in (d)). The signal that might be residually contaminated by the cardiac-field artefact appears in lighter colour (not included in the analysis). The grey area highlights the time window in which a significant trial-by-trial correlation between HER amplitude and ‘Me’ ratings was observed. (b) HER amplitude in the significant time window plotted against ‘Me’ ratings. Each point represents one trial. (c) Mean Pearson correlation coefficient in the 304–354 ms time window, along the different recording sites of the electrode shaft of patient 1. The black bar corresponds to the recording site for which a significant correlation was found. (d) Differential HERs, sympathetic regulation and vmPFC. Recording site 2 (circled dot) showed the significant correlation, while recording site 1 and the triangle (patient 2) showed no effect. Regions in red showed differential responses to heartbeats along the ‘Me’ scale, in a previous MEG study [25]. Regions in green are involved in sympathetic regulation [34]. Yellow corresponds to the overlap between MEG results and sympathetic regulation regions.

Figure 4.

The trial-by-trial amplitude of HERs in the ventral precuneus and vPCC correlates with the involvement of the ‘I’ in spontaneous thoughts (patient 4). (a) Time course of the Pearson correlation coefficient r between the trial-by-trial HER amplitude and the ratings on the ‘I’ scale (black), and HERs (±s.e.m.) for ‘high’ (dark blue) and ‘low’ (light blue) ratings on the ‘I’ scale (median split of ratings), for recording site 1. The signal that might be residually contaminated by the cardiac-field artefact appears in lighter colour (not included in the analysis). The grey area highlights the time window in which a significant trial-by-trial correlation between HER amplitude and ‘I’ ratings was observed. (b) HER amplitude in the significant time window plotted against ‘I’ rating. Each point represents one trial. (c) Mean Pearson correlation coefficient in the 444–500 ms time window, along the different recording sites of the electrode shaft. The black bar corresponds to the recording site for which a significant correlation was found. (d) Differential HERs, parasympathetic regulation and posteromedial cortex. The circled dot indicates the location of recording site 1. Regions in blue showed differential responses to heartbeats along the ‘I’ scale, in a previous MEG study [25]. Regions in green are involved in parasympathetic regulation [34]. Outlines correspond to the parcellation of the posteromedial cortex [32]: ventral precuneus (vPrc, dark pink), dorsal cingulate (dPCC, light pink) and ventral cingulate cortex (vPCC, pink).

Figure 5.

The amplitude of HERs in the rAI correlates with the involvement of the ‘I’ in spontaneous thoughts, in MEG (panels a–e) and in iEEG (panels f–j). (a) Sagittal view of the insula with three insular sub-regions [30] highlighted: PI (light pink), dAI (pink), vAI (dark pink). Light green and dark green regions are associated with parasympathetic and sympathetic regulation respectively [34]. (b–d) Time course of the HER (±s.e.m. across the 16 participants) for ‘high’ and ‘low’ responses on the ‘I’ scale (median split of responses), for the three ROIs in MEG source analysis. The grey area highlights the time window where a significant difference between HERs for ‘high’ and ‘low’ ratings on the ‘I’ scale was observed. (e) Differential MEG source activity for ‘high’ versus ‘low’ ratings on the ‘I’ scale averaged over 384–480 ms post R-peak (threshold for visualization: uncorrected p < 0.05; 75% smoothness applied to the cortical surface). The pink region corresponds to the rAI (union of dAI and vAI). (f) Axial view of the right hemisphere showing the PI (light pink) and dAI (pink). Black dots correspond to the two recording sites analysed in patient 3. Recording site 2 (circled dot) showed a significant correlation between HER amplitude and ‘I’ ratings, in a time window consistent with the MEG results. Areas in green are involved in parasympathetic regulation [34]. (g) Time course of the trial-by-trial Pearson correlation coefficient r between HER amplitude and ‘I’ ratings (black), and HERs (±s.e.m) for ‘high’ (dark blue) and ‘low’ (light blue) ratings on the ‘I’ scale (median split of responses), for recording site 2 of patient 3 (circled dot in f). The grey area highlights the time window in which a significant correlation between HER amplitude and ‘I’ ratings was observed. (h) HER amplitude in the significant time window plotted against ‘I’ ratings. Each point represents one trial. (i) Mean Pearson correlation coefficient in the 397–443 ms time window, along the different recording sites of the electrode shaft of patient 3. (j) Axial view of the right hemisphere showing the PI (light pink) and dAI (pink), for patient 5. The black dot corresponds to the recording site analysed for this patient, where no significant correlation was observed.

Figure 6.

Comparison of effects in the insula and in the DN. Source activity was averaged for each significant time window, across the significant vertices (vmPFC: left, vPrc/vPCC: middle) or across the vertices belonging to the rAI ROI (right).