Exteroceptive expectations modulate interoceptive processing: repetition-suppression effects for visual and heartbeat evoked potentials

Abstract

Interoception refers to the signaling of internal bodily commands. Here, we explore repetition suppression of intero- and exteroceptive neural markers to test whether the perception and predictability of exteroceptive stimulus material affects their expression. Participants completed a repetition suppression paradigm in which angry or neutral facial expressions repeated or alternated. Participants received either an implicit (experiment 1) or explicit (experiment 2) cue enabling the formation of expectations regarding the upcoming facial expression. We measured the heartbeat-evoked potential (HEP) indexing cardiac processing and visual evoked potentials (VEP) in response to viewing the second (repeated or alternated) face. Repeating angry facial expressions produced repetition suppression of both HEP and VEP amplitude while repeating neutral expressions led to repetition enhancement of HEP amplitude. This effect was magnified when participants were explicitly aware of predictive cues. Furthermore, repetition suppression of HEP amplitude correlated with neural attenuation of VEP activity. Results highlight repetition effects for interoceptive as well as exteroceptive neural markers and support top-down, expectation-based accounts of the phenomenon. Furthermore, results demonstrate that the perception of exteroceptive stimulus information has an effect on the processing of interoceptive signals and suggest a direct neural connection between the processing of external and internal sensory information.

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

“…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.…”

“…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.…”

“…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).…”

“…Accordingly, it seems perhaps counterintuitive that predictive information about negative affective material may not facilitate but interfere with interoceptive processing (see Marshall et al, 2017 for a complementary explanation on the attentional bias hypothesis). Furthermore, the current findings are in line with evidence demonstrating the influence of affective valence on visceromotor response.…”

“…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.…”