Attention, in and Out: Scalp-Level and Intracranial EEG Correlates of Interoception and Exteroception

Abstract

Interoception, the monitoring of visceral signals, is often presumed to engage attentional mechanisms specifically devoted to inner bodily sensing. In fact, most standardized interoceptive tasks require directing attention to internal signals. However, most studies in the field have failed to compare attentional modulations between internally- and externally-driven processes, thus probing blind to the specificity of the former. Here we address this issue through a multidimensional approach combining behavioral measures, analyses of event-related potentials and functional connectivity via high-density electroencephalography, and intracranial recordings. In Study 1, 50 healthy volunteers performed a heartbeat detection task as we recorded modulations of the heartbeat-evoked potential (HEP) in three conditions: exteroception, basal interoception (also termed interoceptive accuracy), and post-feedback interoception (sometimes called interoceptive learning). In Study 2, to evaluate whether key interoceptive areas (posterior insula, inferior frontal gyrus, amygdala, and somatosensory cortex) were differentially modulated by externally- and internally-driven processes, we analyzed human intracranial recordings with depth electrodes in these regions. This unique technique provides a very fine grained spatio-temporal resolution compared to other techniques, such as EEG or fMRI. We found that both interoceptive conditions in Study 1 yielded greater HEP amplitudes than the exteroceptive one. In addition, connectivity analysis showed that post-feedback interoception, relative to basal interoception, involved enhanced long-distance connections linking frontal and posterior regions. Moreover, results from Study 2 showed a differentiation between oscillations during basal interoception (broadband: 35–110 Hz) and exteroception (1–35 Hz) in the insula, the amygdala, the somatosensory cortex, and the inferior frontal gyrus. In sum, this work provides convergent evidence for the specificity and dynamics of attentional mechanisms involved in interoception.

Heart-Brain Interactions Shape Somatosensory Perception and Evoked Potentials

“…Similar modulation of early SEP components (P50) has previously been shown along with shifts of spatial attention (Forschack et al, 2017;Schubert et al, 2008). Given that HEP amplitude has been found to be significantly higher during interoceptive compared to exteroceptive attention (García-Cordero et al, 2017;Petzschner et al, 2019;Villena-González et al, 2017), we propose that the modulations of HEP amplitude reflect attentional shifts between external stimuli (exteroception) and internal bodily states (interoception). In line with this view, it has been suggested that the sudden ''ignition'' of a spontaneous internal activity can block external sensory processing (Dehaene & Changeux, 2005).…”

Skipping a beat: heartbeat-evoked potentials reflect predictions during interoceptive-exteroceptive integration

“…Consistent with the characterisation of the HEP as a neural correlate of precision-weighted interoceptive prediction error, many studies have reported attentional modulation of the amplitude of the HEP -for example, during tasks involving attending to heartbeat sensations relative to external stimuli (García-Cordero et al, 2017;Montoya, Schandry, & Müller, 1993;Petzschner et al, 2019;Schandry et al, 1986;Villena-González et al, 2017;Yuan, Yan, Xu, Han, & Yan, 2007).…”

Altered neural signatures of interoception in multiple sclerosis

“…As expected, given these previous inconsistencies, we found no differences between groups in any of them (see Supporting Information Data S1 and Supporting Information Table S1). More particularly, HEP modulations have been widely shown to be autonomously reliable as a robust index of general attention to body-inner sensations (Garcia-Cordero et al, 2017;Garcia-Cordero et al, 2016;Pollatos & Schandry, 2004;Yoris, Abrevaya, et al, 2018;Yoris, García, Traiber, Santamaría-García, Esteves, et al, 2017;Yoris, García, Traiber, Santamaría-García, Martorell, et al, 2017) as well as other processes associated with body-brain communication, such as body awareness (Muller et al, 2015), emotional experience (Couto, Aldofi, Velasquez, et al, 2015), motivation (Weitkunat, 1990), attention (Montoya, Schandry, & Muller, 1993), and pain perception (Shao, Shen, Wilder-Smith, & Li, 2011). More particularly, HEP modulations have been widely shown to be autonomously reliable as a robust index of general attention to body-inner sensations (Garcia-Cordero et al, 2017;Garcia-Cordero et al, 2016;Pollatos & Schandry, 2004;Yoris, Abrevaya, et al, 2018;Yoris, García, Traiber, Santamaría-García, Esteves, et al, 2017;Yoris, García, Traiber, Santamaría-García, Martorell, et al, 2017) as well as other processes associated with body-brain communication, such as body awareness (Muller et al, 2015), emotional experience (Couto, Aldofi, Velasquez, et al, 2015), motivation (Weitkunat, 1990), attention (Montoya, Schandry, & Muller, 1993), and pain perception (Shao, Shen, Wilder-Smith, & Li, 2011).…”

“…Thus, following previous studies (Muller et al, 2015;Schulz et al, 2015), we focused our main analysis on HEP modulations, which provide critical information about the temporal dynamics of interoception. More particularly, HEP modulations have been widely shown to be autonomously reliable as a robust index of general attention to body-inner sensations (Garcia-Cordero et al, 2017;Garcia-Cordero et al, 2016;Pollatos & Schandry, 2004;Yoris, Abrevaya, et al, 2018;Yoris, García, Traiber, Santamaría-García, Esteves, et al, 2017;Yoris, García, Traiber, Santamaría-García, Martorell, et al, 2017) as well as other processes associated with body-brain communication, such as body awareness (Muller et al, 2015), emotional experience (Couto, Aldofi, Velasquez, et al, 2015), motivation (Weitkunat, 1990), attention (Montoya, Schandry, & Muller, 1993), and pain perception (Shao, Shen, Wilder-Smith, & Li, 2011). These properties highlight the relevance of the HEP as a reliable and self-sufficient nonbehavioral subclinical measure to afford critical insights of the cortical monitoring of internal signals.…”

“…done in previous reports, to avoid redundant comparisons and get a robust signal per condition(Garcia-Cordero et al, 2017;Garcia-Cordero et al, 2016;Yoris, Abrevaya, et al, 2018;Yoris, García, Traiber, Santamaría-García, Esteves, et al, 2017;Yoris, García, Traiber, Santamaría-García, Martorell, et al, 2017). This permutation analysis is a robust approach to EEG data which has been applied in several studies assessing modulations of the HEPCouto, Adolfi, Velasquez, et al, 2015;Couto et al, 2014;Craig, 2002;Critchley & Harrison, 2013;Critchley, Wiens, Rotshtein, Ohman, & Dolan, 2004;Garcia-Cordero et al, 2016) and other ERPs(Amoruso et al, 2014;Chennu et al, 2013;Gonzalez-Gadea et al, 2015;Ibanez et al, 2013;Melloni et al, 2015;Melloni et al, 2016).This method gives a straightforward solution for the multiple comparison problems and does not depend on multiple comparison corrections or Gaussian distribution assumptions.…”