Neural responses to heartbeats distinguish self from other during imagination

Abstract

Imagination is an internally-generated process, where one can make oneself or other people appear as protagonists of a scene. How does the brain tag the protagonist of an imagined scene as being oneself or someone else? Crucially, during imagination, neither external stimuli nor motor feedback are available to disentangle imagining oneself from imagining someone else. Here, we test the hypothesis that an internal mechanism based on the neural monitoring of heartbeats could distinguish between self and other. 23 participants imagined themselves (from a first-person perspective) or a friend (from a third-person perspective) in various scenarios, while their brain activity was recorded with magnetoencephalography and their cardiac activity was simultaneously monitored. We measured heartbeat-evoked responses, i.e. transients of neural activity occurring in response to each heartbeat, during imagination. The amplitude of heartbeat-evoked responses differed between imagining oneself and imagining a friend, in the precuneus and posterior cingulate regions bilaterally. Effect size was modulated by the daydreaming frequency scores of participants but not by their interoceptive abilities. These results could not be accounted for by other characteristics of imagination (e.g., the ability to adopt the perspective, valence or arousal), nor by cardiac parameters (e.g., heart rate) or arousal levels (e.g. arousal ratings, pupil diameter). Heartbeat-evoked responses thus appear as a neural marker distinguishing self from other during imagination.

Visceral Signals Shape Brain Dynamics and Cognition

“…A patient with insular lesions could perform well at interoceptive tasks provided that cardiac-related inputs mediated by the skin were available ( [175], but see also [176]). In addition, functionally relevant HERs were observed predominantly outside the insula in several experiments [111,128,130,131,135] ( Figure 5).…”

“…(F) Confirmation of the findings in intracranial recordings in vmPFC, with a correlation between single-trial HERs and 'Me' ratings. Another study revealed that HERs distinguish between self and other [135]. (G-I) HERs predict visual perception at threshold [111].…”

“…In this experiment HERs did not vary with the emotional valence of spontaneous thoughts, showing that HERs can covary with aspects of cognition that are not related to emotions. Another study revealed that HERs in medial regions partially overlapping the default network distinguish between self and other [135].…”

Understanding Neural Oscillations in the Human Brain: From Movement to Consciousness and Vice Versa

“…A significant correlation between the global field alpha power and respiration was demonstrated in the eyes-closed resting state (Yuan et al, 2013). Other internal (visceral) movements, such as heartbeats, contribute not only to the DMN state, but also to encoding the self (Babo-Rebelo et al, 2016, 2019; Azzalini et al, 2019). The relative permanency of the self-referential and time to time modulation of mind wandering (Smallwood and Schooler, 2015; Kucyi, 2018) should be taken into account as a basic experimental control for the measurement of conscious events (Northoff et al, 2010).…”

Heartbeat-evoked potentials during interoceptive-exteroceptive integration are not consistent with precision-weighting

“…As recommended by SPM12, we low-pass filtered the resulting HEP below 20Hz (again, with EEGLAB’s pop_neweegfilt). In deviation from our pre-registration, but following discussions with peer reviewers and investigation of similar decisions in previous studies of HEPs (Azzalini et al, 2019; Babo-Rebelo et al, 2016, 2019; Banellis & Cruse, 2020; Park et al, 2014; Petzschner et al, 2019), we chose not to apply any baseline correction to our data as cardiac activity is cyclical by nature and may therefore insert artefactual effects in post-R data. This decision also allows direct comparison with published results of Banellis and Cruse (2020).…”