Increased functional connectivity between superior colliculus and brain regions implicated in bodily self‐consciousness during the rubber hand illusion

Olivé, Isadora; Tempelmann, Claus; Berthoz, Alain; Heinze, Hans-Joachim

doi:10.1002/hbm.22659

Cited by 25 publications

(23 citation statements)

References 64 publications

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“…Thus, our data suggest that the amygdala may play an important role in multisensory integration of temporally congruent tactile, visual, and proprioceptive information (i.e., bottom-up processes in the RHI) or may be involved in the integration of external stimuli into one's own body representation (i.e., top-down processes in the RHI; Marotta et al, 2016). Importantly, the observation that a complete absence of the RHI in a subsample of five participants was not associated with significantly larger amygdala volumes underscores the importance of multisensory integration in other brain areas like the premotor cortex (Ehrsson et al, 2004) or the temporoparietal junction (Olivé et al, 2015). Further studies are needed to gain mechanistic insights into the amygdala's function in illusory experiences and to elucidate neural networks involved in not only the emergence but also the prevention of body illusions.…”

Section: Discussionmentioning

confidence: 87%

A Protective Mechanism against Illusory Perceptions Is Amygdala-Dependent

et al. 2019

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Most people have a clear sense of body ownership, preserving them from physical harm. However, perceptual body illusions -famously the rubber hand illusion (RHI) -can be elicited experimentally in healthy individuals. We hypothesize that the amygdala, a core component of neural circuits of threat processing, is involved in protective mechanisms against disturbed body perceptions. To test this hypothesis, we started by investigating two monozygotic human twin sisters with focal bilateral amygdala damage due to Urbach-Wiethe disease. Relative to 20 healthy women, the twins exhibited, on two occasions 1 year apart, augmented RHI responses in form of faster illusion onset and increased vividness ratings. Following up on these findings, we conducted a volumetric brain morphometry study involving an independent, gender-mixed sample of 57 healthy human volunteers (36 female, 21 male). Our results revealed a positive correlation between amygdala volume and RHI onset, i.e., the smaller the amygdala, the less time it took the RHI to emerge. This raised the question of whether a similar phenotype would result from experimental amygdala inhibition. To dampen amygdala reactivity, we intranasally administered the peptide hormone oxytocin to the same 57 individuals in a randomized trial before conducting the RHI. Compared with placebo, oxytocin treatment yielded enhanced RHI responses, again evident in accelerated illusion onset and increased vividness ratings. Together, the present series of experiments provides converging evidence for the amygdala's unprecedented role in reducing susceptibility to the RHI, thus protecting the organism from the potentially fatal threats of a distorted bodily self. Significance StatementCompelling evidence indicates that the amygdala is of vital importance for danger detection and fear processing. However, lethal threats can arise not only from menacing external stimuli but also from distortions in bodily self-perception. Intriguingly, the amygdala's modulatory role in such illusory body perceptions is still elusive. To probe the amygdala's involvement in illusory body experiences, we conducted a multi-methodological series of experiments in a rare human amygdala lesion model, complemented by a morphological and pharmaco-modulatory experiment in healthy volunteers. Our findings convergently suggest that the amygdala's integrity is indispensable for maintaining an unbiased, precise perception of our bodily self. Hence, the amygdala might shield us against distortions in self-perception and the resultant loss of behavioral control of our organism.

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Section: Discussionmentioning

confidence: 87%

A Protective Mechanism against Illusory Perceptions Is Amygdala-Dependent

et al. 2019

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“…The right TPJ, has been associated extensively with bodily self‐consciousness in illusion studies conducted in healthy individuals, as well as in neurological patients [Blanke et al, ; Heydrich et al, ], and has been repeatedly associated with out‐of‐body experiences [Arzy et al, ; Heydrich et al, ], the latter being the defining symptom of the dissociative subtype [Lanius et al, ]. Here, one study reported specifically an increase in functional connectivity between the SC and right TPJ during an illusion paradigm manipulating body‐part ownership [Olive et al, ], the rubber hand illusion, which recently was shown to evoke strong responses in PTSD + DS patients [Hirschmann and Lev‐Ari, ; Rabellino et al, ].…”

Section: Discussionmentioning

confidence: 78%

“…When contrasting the PTSD + DS to the PTSD group, we observed increased functional connectivity between the SC and the rTPJ. The right TPJ has been shown previously to play a critical role in bodily self‐consciousness [Ionta et al, ; Olive et al, ]. The right TPJ, has been associated extensively with bodily self‐consciousness in illusion studies conducted in healthy individuals, as well as in neurological patients [Blanke et al, ; Heydrich et al, ], and has been repeatedly associated with out‐of‐body experiences [Arzy et al, ; Heydrich et al, ], the latter being the defining symptom of the dissociative subtype [Lanius et al, ].…”

Section: Discussionmentioning

confidence: 99%

“…The forward deformation fields were generated and used to spatially normalize the functional images to MNI space. In keeping with a previous SC functional neuroimaging study [Olive et al, ], the images were then smoothed with a three‐dimensional isotropic Gaussian kernel of 6mm FWHM (full‐width at half maximum). The smoothed functional images were further motion corrected with ART software [Gabrieli Lab, McGovern Institute for Brain Research, Cambridge, MA], which generates outlier motion regressors that were used as a covariate of no interest during within‐subject (first‐level) analysis.…”

Section: Methodsmentioning

confidence: 99%

“…These findings suggest a strong linkage between hypervigilant behaviour and fast fight‐or‐flight active defensive responses operant at the SC [Kozlowska et al, ]. Notably, a previous study [Olive et al, ] points further to the role of the SC in passive defensive responses, characterized by detachment of emotion and anomalous bodily experience, including feelings of distortion of the body size, mass or shape, and out‐of‐body experiences [Lanius et al, ].…”

Section: Introductionmentioning

confidence: 99%

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Superior colliculus resting state networks in post‐traumatic stress disorder and its dissociative subtype

Olivé

Densmore

Harricharan

et al. 2017

Human Brain Mapping

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Objectives: The innate alarm system (IAS) models the neurocircuitry involved in threat processing in posttraumatic stress disorder (PTSD). Here, we investigate a primary subcortical structure of the IAS model, the superior colliculus (SC), where the SC is thought to contribute to the mechanisms underlying threat-detection in PTSD. Critically, the functional connectivity between the SC and other nodes of the IAS remains unexplored. Experimental design: We conducted a resting-state fMRI study to investigate the functional architecture of the IAS, focusing on connectivity of the SC in PTSD (n 5 67), its dissociative subtype (n 5 41), and healthy controls (n 5 50) using region-of-interest seed-based analysis. Principal observations: We observed group-specific resting state functional connectivity between the SC for both PTSD and its dissociative subtype, indicative of dedicated IAS collicular pathways in each group of patients. When comparing PTSD to its dissociative subtype, we observed increased resting state functional connectivity between the left SC and the right dorsolateral prefrontal cortex (DLPFC) in PTSD. The DLPFC is involved in modulation of emotional processes associated with active defensive responses characterising PTSD. Moreover, when comparing PTSD to its dissociative subtype, increased resting state functional connectivity was observed between the right SC and the right temporoparietal junction in the dissociative subtype. The temporoparietal junction is involved in depersonalization responses associated with passive defensive responses typical of the dissociative subtype. Conclusions: Our findings suggest that unique resting state functional connectivity of the SC parallels the unique symptom profile and defensive responses observed in PTSD and its dissociative subtype.

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Approaches to Understanding Multisensory Dysfunction in Autism Spectrum Disorder

2020

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Abnormal sensory responses are a DSM‐5 symptom of autism spectrum disorder (ASD), and research findings demonstrate altered sensory processing in ASD. Beyond difficulties with processing information within single sensory domains, including both hypersensitivity and hyposensitivity, difficulties in multisensory processing are becoming a core issue of focus in ASD. These difficulties may be targeted by treatment approaches such as “sensory integration,” which is frequently applied in autism treatment but not yet based on clear evidence. Recently, psychophysical data have emerged to demonstrate multisensory deficits in some children with ASD. Unlike deficits in social communication, which are best understood in humans, sensory and multisensory changes offer a tractable marker of circuit dysfunction that is more easily translated into animal model systems to probe the underlying neurobiological mechanisms. Paralleling experimental paradigms that were previously applied in humans and larger mammals, we and others have demonstrated that multisensory function can also be examined behaviorally in rodents. Here, we review the sensory and multisensory difficulties commonly found in ASD, examining laboratory findings that relate these findings across species. Next, we discuss the known neurobiology of multisensory integration, drawing largely on experimental work in larger mammals, and extensions of these paradigms into rodents. Finally, we describe emerging investigations into multisensory processing in genetic mouse models related to autism risk. By detailing findings from humans to mice, we highlight the advantage of multisensory paradigms that can be easily translated across species, as well as the potential for rodent experimental systems to reveal opportunities for novel treatments. Lay Summary Sensory and multisensory deficits are commonly found in ASD and may result in cascading effects that impact social communication. By using similar experiments to those in humans, we discuss how studies in animal models may allow an understanding of the brain mechanisms that underlie difficulties in multisensory integration, with the ultimate goal of developing new treatments. Autism Res 2020, 13: 1430–1449. © 2020 International Society for Autism Research, Wiley Periodicals, Inc.

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Increased functional connectivity between superior colliculus and brain regions implicated in bodily self‐consciousness during the rubber hand illusion

Cited by 25 publications

References 64 publications

A Protective Mechanism against Illusory Perceptions Is Amygdala-Dependent

A Protective Mechanism against Illusory Perceptions Is Amygdala-Dependent

Superior colliculus resting state networks in post‐traumatic stress disorder and its dissociative subtype

Approaches to Understanding Multisensory Dysfunction in Autism Spectrum Disorder

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