The Insula Mediates Access to Awareness of Visual Stimuli Presented Synchronously to the Heartbeat

Salomon, Roy; Ronchi, Roberta; Dönz, Jonathan; Bello-Ruiz, Javier; Herbelin, Bruno; Martet, Remi; Faivre, Nathan; Schaller, Karl; Blanke, Olaf

doi:10.1523/jneurosci.4262-15.2016

Cited by 147 publications

(146 citation statements)

References 82 publications

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“…Our study not only shows commonalities among the brain networks linked to MSI, but it also demonstrates sensory‐specific integration effects. Consistent with the fMRI literature with respect to unisensory processing, we observed activation in the amygdala during olfactory processing (e.g., Seubert et al, ), activation of the STG as well as the IFG and the dorsomedial prefrontal cortex (dmPFC) during auditory stimulation, and activation of the striate/extrastriate visual areas, the dmPFC and the insula/IFG during visual stimulation (e.g., Costafreda, Brammer, David, & Fu, ; Nourski, ; Salomon et al, ). Examining the network linked to the integration of visual and olfactory information (OV > O + V), we observed activation in the amygdala, the putamen and the caudate, which dropped out at the conjunction with the respective contrast for audio–visual integration.…”

Section: Discussionsupporting

confidence: 88%

Audio–visual and olfactory–visual integration in healthy participants and subjects with autism spectrum disorder

Stickel

Weismann

Kellermann

et al. 2019

Human Brain Mapping

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The human capacity to integrate sensory signals has been investigated with respect to different sensory modalities. A common denominator of the neural network underlying the integration of sensory clues has yet to be identified. Additionally, brain imaging data from patients with autism spectrum disorder (ASD) do not cover disparities in neuronal sensory processing. In this fMRI study, we compared the underlying neural networks of both olfactory–visual and auditory–visual integration in patients with ASD and a group of matched healthy participants. The aim was to disentangle sensory‐specific networks so as to derive a potential (amodal) common source of multisensory integration (MSI) and to investigate differences in brain networks with sensory processing in individuals with ASD. In both groups, similar neural networks were found to be involved in the olfactory–visual and auditory–visual integration processes, including the primary visual cortex, the inferior parietal sulcus (IPS), and the medial and inferior frontal cortices. Amygdala activation was observed specifically during olfactory–visual integration, with superior temporal activation having been seen during auditory–visual integration. A dynamic causal modeling analysis revealed a nonlinear top‐down IPS modulation of the connection between the respective primary sensory regions in both experimental conditions and in both groups. Thus, we demonstrate that MSI has shared neural sources across olfactory–visual and audio–visual stimulation in patients and controls. The enhanced recruitment of the IPS to modulate changes between areas is relevant to sensory perception. Our results also indicate that, with respect to MSI processing, adults with ASD do not significantly differ from their healthy counterparts.

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Section: Discussionsupporting

confidence: 88%

Audio–visual and olfactory–visual integration in healthy participants and subjects with autism spectrum disorder

Stickel

Weismann

Kellermann

et al. 2019

Human Brain Mapping

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“…Our hypotheses are in line with the main idea that sensory processing of external cues is influenced by internal bodily states (Barrett & Simmons, 2015;Salomon et al, 2016). To this aim, the repetition suppression paradigm was modified to include not only neutral but also affective stimuli, and stimulus repetition was varied with respect to this valence dimension, as opposed to repetition of lowlevel features (i.e., identity repetition).…”

Section: Introductionsupporting

confidence: 59%

“…In brief, data were submitted to a repeated measures, two-tailed cluster mass permutation test (Bullmore et al, 1999) using a family-wise alpha level of 0.05 (i.e., 5,226 total comparisons). Where appropriate, we calculated Bayesian statistics for null effects (Babo-Rebelo et al, 2016;Park et al, 2017;Rouder, Speckman, Sun, Morey, & Iverson, 2009;Salomon et al, 2016) using the online Bayes factor calculation tool (http://pcl. Repeated measures t tests were performed for each comparison using the original data and 2,500 random within-participant permutations of the data.…”

Section: Hep Amplitudementioning

confidence: 99%

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

Gentsch

Sel

Marshall

et al. 2018

Human Brain Mapping

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The perception of internal bodily signals (interoception) is central to many theories of emotion and embodied cognition. According to recent theoretical views, the sensory processing of visceral signals such as one's own heartbeat is determined by top-down predictions about the expected interoceptive state of the body (interoceptive inference). In this EEG study we examined neural responses to heartbeats following expected and unexpected emotional stimuli. We used a modified stimulus repetition task in which pairs of facial expressions were presented with repeating or alternating emotional content, and we manipulated the emotional valence and the likelihood of stimulus repetition. We found that affective predictions of external socially relevant information modulated the heartbeat-evoked potential, a marker of cardiac interoception. Crucially, the HEP changes highly relied on the expected emotional content of the facial expression. Thus, expected negative faces led to a decreased HEP amplitude, whereas such an effect was not observed after an expected neutral face. These results suggest that valence-specific affective predictions, and their uniquely associated predicted bodily sensory state, can reduce or amplify cardiac interoceptive responses. In addition, the affective repetition effects were dependent on repetition probability, highlighting the influence of top-down exteroceptive predictions on interoception. Our results are in line with recent models of interoception supporting the idea that predicted bodily states influence sensory processing of salient external information.

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“…Besides modulating arterial baroreceptor discharge, heartbeat-related pressure fluctuations generate periodic sensory influences throughout the body-affecting, for example, the discharge of tactile (Macefield, 2003) or muscle spindle afferents (Birznieks, Boonstra, & Macefield, 2012)-which are predicted and normally do not enter perceptual awareness. In our constant attempt to minimize sensory uncertainty (Peters, McEwen, & Friston, 2017), inhibition of such predictable cardiac-induced sensory effects has been argued to reducepotentially distracting-self-related sensory noise (Salomon et al, 2016) at the benefit of our processing of the outside world, for example, by increasing the signal-to-noise ratio of external stimuli. Correspondingly, stimuli presented simultaneously with the heartbeat are interpreted as sensory consequences of the organism's own (internal) cardiac activity and thus perceptually attenuated (Salomon et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Active information sampling varies across the cardiac cycle

et al. 2019

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Perception and cognition oscillate with fluctuating bodily states. For example, visual processing has been shown to change with alternating cardiac phases. Here, we study the heartbeat's role for active information sampling-testing whether humans implicitly act upon their environment so that relevant signals appear during preferred cardiac phases. During the encoding period of a visual memory experiment, participants clicked through a set of emotional pictures to memorize them for a later recognition test. By self-paced key press, they actively prompted the onset of short (100 ms) presented pictures. Simultaneously recorded electrocardiograms allowed us to analyze the self-initiated picture onsets relative to the heartbeat. We find that self-initiated picture onsets vary across the cardiac cycle, showing an increase during cardiac systole, while memory performance was not affected by the heartbeat. We conclude that active information sampling integrates heart-related signals, thereby extending previous findings on the association between body-brain interactions and behavior. K E Y W O R D Scardiovascular, emotion, interoception, memory, sensation/perception, young adults 2 of 16 | KUNZENDORF Et al. Cardiac activity occurs in a cycle of two phases: During diastole, the ventricles relax to be filled with blood; during systole, the ventricles contract and eject blood into the arteries, while visceral pathways send information about each heartbeat to the brain (Critchley & Harrison, 2013). Such natural phasic changes of the cardiovascular state have been mainly associated with variations in perception. For sensory processing, which is typically measured with detection tasks or reaction time tasks, response to passively presented stimuli has been shown to be attenuated during early cardiac phases (i.e., during systole) or relatively enhanced at later time points in the cardiac cycle (i.e., at diastole;

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The Insula Mediates Access to Awareness of Visual Stimuli Presented Synchronously to the Heartbeat

Cited by 147 publications

References 82 publications

Audio–visual and olfactory–visual integration in healthy participants and subjects with autism spectrum disorder

Audio–visual and olfactory–visual integration in healthy participants and subjects with autism spectrum disorder

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

Active information sampling varies across the cardiac cycle

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