Cardiac interoceptive learning is modulated by emotional valence perceived from facial expressions

Abstract

Interoception refers to the processing of homeostatic bodily signals. Research demonstrates that interoceptive markers can be modulated via exteroceptive stimuli and suggests that the emotional content of this information may produce distinct interoceptive outcomes. Here, we explored the impact of differently valenced exteroceptive information on the processing of interoceptive signals. Participants completed a repetition-suppression paradigm viewing repeating or alternating faces. In experiment 1, faces wore either angry or pained expressions to explore the interoceptive response to different types of negative stimuli in the observer. In experiment 2, expressions were happy or sad to compare interoceptive processing of positive and negative information. We measured the heartbeat evoked potential (HEP) and visual evoked potentials (VEPs) as a respective marker of intero- and exteroceptive processing. We observed increased HEP amplitude to repeated sad and pained faces coupled with reduced HEP and VEP amplitude to repeated angry faces. No effects were observed for positive faces. However, we found a significant correlation between suppression of the HEP and VEP to repeating angry faces. Results highlight an effect of emotional expression on interoception and suggest an attentional trade-off between internal and external processing domains as a potential account of this phenomenon.

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

“…In the current study, affective repetition effects on cardiac interoceptive processing were only observed in repetition blocks, suggesting that the repetition effects were highly dependent on probability context. Our results are in line with previous evidence that highlight the role of expectations in repetition effects (Marshall et al, 2017;Marshall et al, 2018) supporting the idea that repetition suppression is a surprise-context-dependent phenomenon that occurs via probability context. The evidence that affective repetition effects were only present when the likelihood of repetitions was high suggests that the HEP modulation may result from global top-down modulation based on probability context (i.e., highrepetition probability) rather than from lower level sources of local prediction signals from the preceding trial.…”

“…These results contrast with previous ERP studies reporting repetition suppression effects on early VEPs (e.g., Engell & McCarthy, 2014;Nemrodov et al, 2015;Vizioli et al, 2010). A recently published ERP study has shown that repetition of the same facial identity posing a negative expression leads to repetition suppression of both VEPs and HEP, in comparison to when posing a neutral expression (Marshall et al, 2017, see also Marshall et al, 2018). By contrast, in our paradigm the repetition manipulation was made in regards to the affective content of the facial expression, that is, emotion component, as opposed to the identity component.…”

“…That is, stimulus repetition of the cue and target face varied with respect to facial affect as opposed to facial identity. This allowed us to directly manipulate the expectation of the facial emotional content independently from putative neural attenuation effects observed in visual processing when low-level visual features are presented in repetition (e.g., Marshall et al, 2017;Marshall et al, 2018;Summerfield et al, 2008). Moreover, we manipulated the likelihood of stimulus repetition by presenting the emotional expressions in two stimulus contexts (blocks).…”

“…Notably, in the exteroceptive domain affective information has been found to influence repetition suppression, with larger effects for negative valence (e.g., fearful faces, Ishai, Pessoa, Bikle, & Ungerleider, 2004;angry prosody, Ethofer et al, 2009) than neutral stimulus material. Furthermore, in two recent studies we were able to show that predicted facial expressions modulated both visual and interoceptive cortical processing in a highly correlated manner (Marshall, Gentsch, Jelin cić, & Schütz-Bosbach, 2017;Marshall, Gentsch, Schröder, & Schütz-Bosbach, 2018). In these studies, the facial identity was kept constant within a given trial, and the repetition manipulation regarded the facial emotion.…”

Visceral Signals Shape Brain Dynamics and Cognition

“…HERs vary with emotions while viewing mood-inducing video clips [122] or while judging the emotional expression of faces [123]. Based on the hypothesis that specific emotions might lead to precise interoceptive predictions [11], the expected repetition of an emotional facial expression leads to a reduction (for angry faces) or increase (for sad or pain faces) in HER amplitude [124,125]. Because emotions are accompanied by changes in bodily parameters, with a linear relationship between heart rate and valence, and between skin conductance and arousal [126], the emotion-related modulations of HERs might reflect either neural responses to changes in bodily state or the cortical mechanisms driving bodily changes [127].…”