Welcoming back my arm: affective touch increases body ownership following right-hemisphere stroke

Paul M Jenkinson; Cristina Papadaki; Sahba Besharati; Valentina Moro; Valeria Gobbetto; Laura Crucianelli; Louise P Kirsch; Renato Avesani; Nick S Ward; Aikaterini Fotopoulou

doi:10.1093/braincomms/fcaa034

Welcoming back my arm: affective touch increases body ownership following right-hemisphere stroke

Brain Commun. 2020 Mar 28;2(1):fcaa034. doi: 10.1093/braincomms/fcaa034. eCollection 2020.

Authors

Paul M Jenkinson¹, Cristina Papadaki², Sahba Besharati^{3

4}, Valentina Moro⁵, Valeria Gobbetto⁵, Laura Crucianelli^{2

6}, Louise P Kirsch^{2

7}, Renato Avesani⁸, Nick S Ward⁹, Aikaterini Fotopoulou²

Affiliations

¹ School of Life and Medical Sciences, University of Hertfordshire, Hatfield AL10 9AB, UK.
² Division of Psychology and Language Science, Research Department of Clinical, Educational and Health Psychology, University College London, London, UK.
³ Department of Psychological Medicine, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁴ Department of Psychology, School of Human and Community Development, University of the Witwatersrand, Johannesburg, South Africa.
⁵ NPSY.Lab_VR, Department of Human Sciences, University of Verona, Verona, Italy.
⁶ Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden.
⁷ Institut des Systèmes Intelligents et de Robotique, Sorbonne Université, Paris, France.
⁸ IRCSS Sacro Cuore Hospital, Negrar, Italy.
⁹ Department of Clinical and Motor Neuroscience, UCL Institute of Neurology, London, UK.

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.

Keywords: DSO; affective touch; body ownership; interoception; multisensory integration.