The inner world of overactive monitoring: neural markers of interoception in obsessive–compulsive disorder

Yoris, Adrián; García, Adolfo M.; Traiber, L.; Santamaría-García, Hernando; Martorell, Miguel; Alifano, Florencia; Kichic, Rafael; Moser, Jason S.; Cetkovich, Marcelo; Manes, Facundo; Ibáñez, Agustín; Sedeño, Lucas

doi:10.1017/s0033291717000368

Cited by 71 publications

(93 citation statements)

References 100 publications

(165 reference statements)

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“…We used a validated HBD task (Melloni et al, 2013; Couto et al, 2014, 2015a; Sedeno et al, 2014; Canales-Johnson et al, 2015; Yoris et al, 2015, 2017; García-Cordero et al, 2016) in which participants are required to tap a computer keyboard along with their heartbeats or external stimuli. First, in the exteroceptive condition, participants were instructed to follow an audio recording of a simulated heartbeat for 2 min.…”

Section: Methodsmentioning

confidence: 99%

“…This simple method, used in previous HEP analyses (Couto et al, 2014, 2015b; Canales-Johnson et al, 2015; García-Cordero et al, 2016; Yoris et al, 2017), offers a straightforward solution for multiple comparison problems and does not depend on Gaussian assumptions about the probability distribution of the data. The data from each comparison between conditions was separately subjected to a random partition and a t -value was then calculated.…”

Section: Methodsmentioning

confidence: 99%

“…For the analysis, we selected a right frontal ROI (Biosemi electrodes 67, 68, 69; Figure 2 ) based on previous reports showing greater HEP amplitudes in right frontal electrodes while subjects paid attention to heartbeats (Schandry et al, 1993; Pollatos and Schandry, 2004; Pollatos et al, 2005; Yoris et al, 2017). Indeed, frontal regions, such as the orbitofrontal cortex, the inferior frontal gyrus, the insula, and the anterior cingulate cortex, have been widely associated with interoception (Craig, 2002, 2009; Critchley et al, 2004; Becker et al, 2015; Hassanpour et al, 2016; Kuehn et al, 2016; Pollatos et al, 2016; Schulz, 2016; Strigo and Craig, 2016).…”

Section: Methodsmentioning

confidence: 99%

“…However, despite this caveat, note that task employed has been previously validated (Melloni et al, 2013; Couto et al, 2014; Sedeno et al, 2014; Canales-Johnson et al, 2015; Yoris et al, 2015, 2017; García-Cordero et al, 2016) and offers a more precise measure of interoceptive performance than other available paradigms (such as mental or discrimination ones) (Yoris et al, 2015). In addition, in our study, differential HEP modulations between interoception and exteroception emerged from a comparison between two motor-tracking conditions, indicating that they were not driven by motor artifacts.…”

Section: Limitationsmentioning

confidence: 99%

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

et al. 2017

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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.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Limitationsmentioning

confidence: 99%

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

et al. 2017

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“…Here, we offer the first direct testing of this hypothesis by examining behavioral, neurophysiological, gray matter volume, and functional connectivity signatures of interoception in healthy subjects and HTD patients without neurocognitive alterations (featuring no cognitive deficits, gray matter abnormalities, or white matter alterations). In particular, our multidimensional approach comprised analyses of (a) behavioral performance on a validated HBD task (Canales‐Johnson et al, ; Couto et al, ; Yoris et al, ); (b) ongoing modulations of the HEP, an electrophysiological cortical signature modulated by attention to cardiac signals (García‐Cordero et al, ; Yoris et al, ; Terhaar et al, ); and (c) neuroimaging recordings, to evaluate anatomical and functional connectivity properties of key interoceptive regions, namely: the insula, the anterior cingulate cortex (ACC), and the somatosensory cortex (Adolfi et al, ; Craig, ; Critchley, Wiens, Rotshtein, Ohman, & Dolan, ; Fukushima, Terasawa, & Umeda, ; Hassanpour et al, ). In light of the above considerations, we predicted that HTD patients would exhibit behavioral interoceptive deficits and alterations in key neural correlates of such a domain.…”

Section: Introductionmentioning

confidence: 99%

Multilevel convergence of interoceptive impairments in hypertension: New evidence of disrupted body–brain interactions

Yoris

Abrevaya

Esteves

et al. 2017

Human Brain Mapping

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Interoception, the sensing of visceral body signals, involves an interplay between neural and autonomic mechanisms. Clinical studies into this domain have focused on patients with neurological and psychiatric disorders, showing that damage to relevant brain mechanisms can variously alter interoceptive functions. However, the association between peripheral cardiac-system alterations and neurocognitive markers of interoception remains poorly understood. To bridge this gap, we examined multidimensional neural markers of interoception in patients with early stage of hypertensive disease (HTD) and healthy controls. Strategically, we recruited only HTD patients without cognitive impairment (as shown by neuropsychological tests), brain atrophy (as assessed with voxel-based morphometry), or white matter abnormalities (as evidenced by diffusion tensor imaging analysis). Interoceptive domains were assessed through (a) a behavioral heartbeat detection task; (b) measures of the heart-evoked potential (HEP), an electrophysiological cortical signature of attention to cardiac signals; and (c) neuroimaging recordings (MRI and fMRI) to evaluate anatomical and functional connectivity properties of key interoceptive regions (namely, the insula and the anterior cingulate cortex). Relative to controls, patients exhibited poorer interoceptive performance and reduced HEP modulations, alongside an abnormal association between interoceptive performance and both the volume and functional connectivity of the above regions. Such results suggest that peripheral cardiac-system impairments can be associated with abnormal behavioral and neurocognitive signatures of interoception. More generally, our findings indicate that interoceptive processes entail bidirectional influences between the cardiovascular and the central nervous systems.

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Altered neural signatures of interoception in multiple sclerosis

Salamone

Esteves

Sinay

et al. 2018

Human Brain Mapping

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Multiple sclerosis (MS) patients present several alterations related to sensing of bodily signals. However, no specific neurocognitive impairment has yet been proposed as a core deficit underlying such symptoms. We aimed to determine whether MS patients present changes in interoception-that is, the monitoring of autonomic bodily information-a process that might be related to various bodily dysfunctions. We performed two studies in 34 relapsing-remitting, early-stage MS patients and 46 controls matched for gender, age, and education. In Study 1, we evaluated the heartbeat-evoked potential (HEP), a cortical signature of interoception, via a 128-channel EEG system during a heartbeat detection task including an exteroceptive and an interoceptive condition. Then, we obtained whole-brain MRI recordings. In Study 2, participants underwent fMRI recordings during two resting-state conditions: mind wandering and interoception. In Study 1, controls exhibited greater HEP modulation during the interoceptive condition than the exteroceptive one, but no systematic differences between conditions emerged in MS patients. Patients presented atrophy in the left insula, the posterior part of the right insula, and the right anterior cingulate cortex, with abnormal associations between neurophysiological and neuroanatomical patterns. In Study 2, controls showed higher functional connectivity and degree for the interoceptive state compared with mind wandering; however, this pattern was absent in patients, who nonetheless presented greater connectivity and degree than controls during mind wandering. MS patients were characterized by atypical multimodal brain signatures of interoception. This finding opens a new agenda to examine the role of inner-signal monitoring in the body symptomatology of MS.

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The inner world of overactive monitoring: neural markers of interoception in obsessive–compulsive disorder

Cited by 71 publications

References 100 publications

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

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

Multilevel convergence of interoceptive impairments in hypertension: New evidence of disrupted body–brain interactions

Altered neural signatures of interoception in multiple sclerosis

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