Abstract
Right-hemisphere stroke can impair the ability to recognize one’s contralesional body parts as belonging to one’s self. The study of this so-called ‘disturbed sense of limb ownership’ can provide unique insights into the neurocognitive mechanisms of body ownership. In this study, we address a hypothesis built upon experimental studies on body ownership in healthy volunteers. These studies have shown that affective (pleasant) touch, an interoceptive modality associated with unmyelinated, slow-conducting C-tactile afferents, has a unique role in the sense of body ownership. In this study, we systematically investigated whether affective touch stimulation could increase body ownership in patients with a disturbed sense of limb ownership following right-hemisphere stroke. An initial feasibility study in 16 adult patients with acute stroke enabled us to optimize and calibrate an affective touch protocol to be administered by the bedside. The main experiment, conducted with a different sample of 26 right hemisphere patients, assessed changes in limb ownership elicited following self- (patient) versus other- (experimenter) generated tactile stimulation, using a velocity known to optimally activate C-tactile fibres (i.e. 3 cm/s), and a second velocity that is suboptimal for C-tactile activation (i.e. 18 cm/s). We further examined the specificity and mechanism of observed changes in limb ownership in secondary analyses looking at (i) the influence of perceived intensity and pleasantness of touch, (ii) touch laterality and (iii) level of disturbed sense of limb ownership on ownership change and (iv) changes in unilateral neglect arising from touch. Findings indicated a significant increase in limb ownership following experimenter-administered, C-tactile-optimal touch. Voxel-based lesion-symptom mapping identified damage to the right insula and, more substantially, the right corpus callosum, associated with a failure to increase body ownership following experimenter-administered, affective touch. Our findings suggest that affective touch can increase the sense of body-part ownership following right-hemisphere stroke, potentially due to its unique role in the multisensory integration processes that underlie the sense of body ownership.
Highlights
Several disturbances of body awareness occur after right-hemisphere stroke, including asomatognosia and somatoparaphrenia
We further examined the specificity and mechanism of observed changes in limb ownership in secondary analyses looking at (1) the influence of perceived intensity and pleasantness of touch, (2) touch laterality, and (3) level of disturbed sense of limb ownership on ownership change, as well as (4) changes in unilateral neglect arising from touch
Our findings suggest that affective touch can increase the sense of body-part ownership following right hemisphere stroke, https://mc.manuscriptcentral.com/braincom potentially due to its unique role in the multisensory integration processes that underlie the sense of body ownership
Summary
Several disturbances of body awareness occur after right-hemisphere stroke, including asomatognosia (i.e. feelings of non-belonging or non-recognition of the limb) and somatoparaphrenia (delusional ideas of disownership; see Jenkinson et al, 2018) These disturbances reveal that our seemingly effortless sense of body ownership (i.e. the sense that my body belongs to me) is supported by distinct neurocognitive mechanisms that warrant scientific study. Existing research into the mechanisms of body ownership in healthy individuals has identified dynamic integration and weighting processes involving several exteroceptive (e.g. vision) and interoceptive signals (i.e. representing the physiological state of the body; see Craig, 2003) Amongst these signals, a specific type of pleasant touch (hereafter referred to as affective touch), plays a significant role (Crucianelli et al, 2013, 2017; Lloyd et al, 2013; van Stralen et al, 2014; Ponzo et al, 2018). Recent work in spinal cordotomy patients suggest some overlap in the processing of hedonic and discriminative aspects of touch (Marshall et al, 2019), and further research is needed to specify the precise contribution of CT and non-CT fibres
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