Dataset Information

Tool-use Extends Peripersonal Space Boundaries in Schizophrenic Patients.

ABSTRACT:

Background and hypothesis

A primary disruption of the bodily self is considered a core feature of schizophrenia (SCZ). The "disembodied" self might be underpinned by inefficient body-related multisensory integration processes, normally occurring in the peripersonal space (PPS), a plastic sector of space surrounding the body whose extent is altered in SCZ. Although PPS is a malleable interface marking the perceptual border between self and others, no study has addressed the potential alteration of its plasticity in SCZ. We investigated the plasticity of PPS in SCZ patients after a motor training with a tool in the far space.

Study design

Twenty-seven SCZ patients and 32 healthy controls (HC) underwent an audio-tactile task to estimate PPS boundary before (Session 1) and after (Session 3) the tool-use. Parameters of PPS, including the size and the slope of the psychometric function describing audio-tactile RTs as a function of the audio-tactile distances, were estimated.

Study results

Results confirm a narrow PPS extent in SCZ. Surprisingly, we found PPS expansion in both groups, thus showing for the first time a preserved PPS plasticity in SCZ. Patients experienced a weaker differentiation from others, as indicated by a shallower PPS slope at Session 1 that correlated positively with negative symptoms. However, at Session 3, patients marked their bodily boundary in a steeper way, suggesting a sharper demarcation of PPS boundaries after the action with the tool.

Conclusions

These findings highlight the importance of investigating the multisensory and motor roots of self-disorders, paving the way for future body-centred rehabilitation interventions that could improve patients' altered body boundary.

SUBMITTER: Ferroni F

PROVIDER: S-EPMC9434469 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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Publications

Tool-use Extends Peripersonal Space Boundaries in Schizophrenic Patients.

Ferroni Francesca F Ardizzi Martina M Magnani Francesca F Ferri Francesca F Langiulli Nunzio N Rastelli Francesca F Lucarini Valeria V Giustozzi Francesca F Volpe Roberto R Marchesi Carlo C Tonna Matteo M Gallese Vittorio V

Schizophrenia bulletin 20220901 5

<h4>Background and hypothesis</h4>A primary disruption of the bodily self is considered a core feature of schizophrenia (SCZ). The "disembodied" self might be underpinned by inefficient body-related multisensory integration processes, normally occurring in the peripersonal space (PPS), a plastic sector of space surrounding the body whose extent is altered in SCZ. Although PPS is a malleable interface marking the perceptual border between self and others, no study has addressed the potential alte ...[more]

PMID: 35708490

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Project description:Stimuli from different sensory modalities occurring on or close to the body are integrated in a multisensory representation of the space surrounding the body, i.e., peripersonal space (PPS). PPS dynamically modifies depending on experience, e.g., it extends after using a tool to reach far objects. However, the neural mechanism underlying PPS plasticity after tool use is largely unknown. Here we use a combined computational-behavioral approach to propose and test a possible mechanism accounting for PPS extension. We first present a neural network model simulating audio-tactile representation in the PPS around one hand. Simulation experiments showed that our model reproduced the main property of PPS neurons, i.e., selective multisensory response for stimuli occurring close to the hand. We used the neural network model to simulate the effects of a tool-use training. In terms of sensory inputs, tool use was conceptualized as a concurrent tactile stimulation from the hand, due to holding the tool, and an auditory stimulation from the far space, due to tool-mediated action. Results showed that after exposure to those inputs, PPS neurons responded also to multisensory stimuli far from the hand. The model thus suggests that synchronous pairing of tactile hand stimulation and auditory stimulation from the far space is sufficient to extend PPS, such as after tool-use. Such prediction was confirmed by a behavioral experiment, where we used an audio-tactile interaction paradigm to measure the boundaries of PPS representation. We found that PPS extended after synchronous tactile-hand stimulation and auditory-far stimulation in a group of healthy volunteers. Control experiments both in simulation and behavioral settings showed that the same amount of tactile and auditory inputs administered out of synchrony did not change PPS representation. We conclude by proposing a simple, biological-plausible model to explain plasticity in PPS representation after tool-use, which is supported by computational and behavioral data.

Project description:The continuous stream of multisensory information between the brain and the body during body-environment interactions is crucial to maintain the updated representation of the perceived dimensions of body parts (metric body representation) and the space around the body (the peripersonal space). Such flow of multisensory signals is often limited by upper limb sensorimotor deficits after stroke. This would suggest the presence of systematic distortions of metric body representation and peripersonal space in chronic patients with persistent sensorimotor deficits. We assessed metric body representation and peripersonal space representation in 60 chronic stroke patients with unilateral upper limb motor deficits, in comparison with age-matched healthy controls. We also administered a questionnaire capturing explicit feelings towards the affected limb. These novel measures were analysed with respect to patients' clinical profiles and brain lesions to investigate the neural and functional origin of putative deficits. Stroke patients showed distortions in metric body representation of the affected limb, characterized by an underestimation of the arm length and an alteration of the arm global shape. A descriptive lesion analysis (subtraction analysis) suggests that these distortions may be more frequently associated with lesions involving the superior corona radiata and the superior frontal gyrus. Peripersonal space representation was also altered, with reduced multisensory facilitation for stimuli presented around the affected limb. These deficits were more common in patients reporting pain during motion. Explorative lesion analyses (subtraction analysis, disconnection maps) suggest that the peripersonal space distortions would be more frequently associated with lesions involving the parietal operculum and white matter frontoparietal connections. Moreover, patients reported altered feelings towards the affected limb, which were associated with right brain damage, proprioceptive deficits and a lower cognitive profile. These results reveal implicit and explicit distortions involving metric body representation, peripersonal space representation and the perception of the affected limb in chronic stroke patients. These findings might have important clinical implications for the longitudinal monitoring and the treatments of often-neglected deficits in body perception and representation.

Dataset Information

Tool-use Extends Peripersonal Space Boundaries in Schizophrenic Patients.

Background and hypothesis

Study design

Study results

Conclusions

Publications

Tool-use Extends Peripersonal Space Boundaries in Schizophrenic Patients.

Similar Datasets

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