Effects of Transcranial Direct Current Stimulation on the Recognition of Bodily Emotions from Point-Light Displays
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Research Collection Journal Article Effects of Transcranial Direct Current Stimulation on the Recognition of Bodily Emotions from Point-Light Displays Author(s): Vonck, Sharona; Swinnen, Stephan P.; Wenderoth, Nicole; Alaerts, Kaat Publication Date: 2015-08 Permanent Link: https://doi.org/10.3929/ethz-b-000107851 Originally published in: Frontiers in Human Neuroscience 9, http://doi.org/10.3389/fnhum.2015.00438 Rights / License: Creative Commons Attribution 4.0 International This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library ORIGINAL RESEARCH published: 03 August 2015 doi: 10.3389/fnhum.2015.00438 Effects of transcranial direct current stimulation on the recognition of bodily emotions from point-light displays Sharona Vonck 1,2, Stephan Patrick Swinnen 1, Nicole Wenderoth 1,3 and Kaat Alaerts 1* 1 Movement Control and Neuroplasticity Research Group, Department of Kinesiology, KU Leuven, Leuven, Belgium, 2 Faculty of Medicine and Life Sciences, Hasselt University, Hasselt, Belgium, 3 Department of Health Sciences and Technology, ETH Zurich, Zurich, Switzerland Perceiving human motion, recognizing actions, and interpreting emotional body language are tasks we perform daily and which are supported by a network of brain areas including the human posterior superior temporal sulcus (pSTS). Here, we applied transcranial direct current stimulation (tDCS) with anodal (excitatory) or cathodal (inhibitory) electrodes mounted over right pSTS (target) and orbito-frontal cortex (reference) while healthy participants performed a bodily emotion recognition task using biological motion point- light displays (PLDs). Performance (accuracy and reaction times) was also assessed on Edited by: a control task which was matched to the emotion recognition task in terms of cognitive Robert Coben, and motor demands. Each subject participated in two experimental sessions, receiving Integrated Neuroscience Services, USA either anodal or cathodal stimulation, which were separated by one week to avoid Reviewed by: residual effects of previous stimulations. Overall, tDCS brain stimulation did not affect Alessio Avenanti, the recognition of emotional states from PLDs. However, when emotions with a negative University of Bologna, Italy or positive–neutral emotional valence were analyzed separately, effects of stimulation Michael A. Nitsche, Georg-August-University, Germany were shown for recognizing emotions with a negative emotional valence (sadness and *Correspondence: anger), indicating increased recognition performance when receiving anodal (excitatory) Kaat Alaerts, stimulation compared to cathodal (inhibitory) stimulation over pSTS. No stimulation effects Movement Control and Neuroplasticity Research Group, were shown for the recognition of emotions with positive–neutral emotional valences. Department of Biomedical These findings extend previous studies showing structure–function relationships between Kinesiology, KU Leuven, Tervuursevest 101, STS and biological motion processing from PLDs and provide indications that stimulation Leuven 3001, Belgium effects may be modulated by the emotional valence of the stimuli. [email protected] Keywords: transcranial direct current stimulation, superior temporal sulcus, emotion recognition, point-light displays, autism, neuromodulation Received: 17 October 2014 Accepted: 17 July 2015 Published: 03 August 2015 Introduction Citation: Vonck S, Swinnen SP, Wenderoth N The human ability to perceive and understand others actions, emotions, and intentions is pivotal to and Alaerts K (2015) Effects of the formation of social interactions, communication, and relationships. At the neural level, studies transcranial direct current stimulation have revealed a set of brain regions which are part of the action perception network or mirror system on the recognition of bodily emotions from point-light displays. and which are particularly involved in human motion perception (Gallese et al., 2004; Rizzolatti and Front. Hum. Neurosci. 9:438. Craighero, 2004; Rizzolatti and Fabbri-Destro, 2008). The existence of “mirror” neurons was first doi: 10.3389/fnhum.2015.00438 described in the macaque monkey brain using single-cell recordings (di Pellegrino et al., 1992). Later, Frontiers in Human Neuroscience | www.frontiersin.org 1 August 2015 | Volume 9 | Article 438 Vonck et al. Can tDCS modulate emotion recognition? neuroimaging and neurophysiological research confirmed the using PLDs. Performance [accuracy and reaction times (RTs)] was existence of a similar “fronto-parietal” mirror system in the also assessed on a control task that was matched to the emotion human brain (Fadiga et al., 1995; Grafton et al., 1996; Iacoboni recognition task in terms of cognitive and motor demands. Each et al., 1999). In addition to the mirror-motor areas in the inferior subject participated in two experimental sessions, receiving either parietal, inferior frontal gyrus and premotor cortex, the action anodal or cathodal stimulation, separated by one week to avoid perception network also encompasses higher-order visual areas in residual effects of previous stimulations. Based on previous studies the posterior superior temporal sulcus (pSTS) that convey visual and in the light of our anatomical hypothesis, we expected anodal input to downstream visuo-motor areas (Rizzolatti and Craighero, (excitatory) stimulation over right pSTS to increase sensitivity to 2004; Caspers et al., 2010; Molenberghs et al., 2010, 2012). Espe- biological motion thereby enhancing emotion recognition abili- cially the right pSTS has been highlighted as a key neural locus ties. Cathodal (inhibitory) tDCS over pSTS is expected to reduce for perception of bodies and biological motion (Allison et al., or have no effect on performance. 2000), as it has been shown to be particularly activated during the perception of eye or mouth movements, body language, and Materials and Methods biological motion (Allison et al., 2000; Hein and Knight, 2008; Redcay, 2008; Carrington and Bailey, 2009). Participants Prior research most frequently adopted the so-called point- Twenty-four subjects participated in the study (15 females, light displays (PLDs) to study the neural basis of biological move- 22.35 0.28 years). All participants were naive regarding the pur- ment perception as they represent a highly controllable, impov- pose of the experiments and were unfamiliar with PLDs. Subjects erished form of biological motion (Johansson, 1973). In these had no history of medical, neurological, or psychiatric disorders, displays, only a few bright moving point-light dots are depicted and none of them were receiving acute or chronic medication against a dark background to represent the movement of the affecting the central nervous system. main joints of a human body. Although they lack any information Written informed consent was obtained from all participants on texture or form, PLDs are highly salient in depicting human prior to the experiment. Consent forms and study design were actions as well as information on the gender or emotional state in approved by the local Ethics Committee for Biomedical Research which the point-light figure is engaged (Johansson, 1973; Cutting at the KU Leuven in accordance to the Code of Ethics of the World and Kozlowski, 1977; Dittrich et al., 1996; Pollick et al., 2002, 2005; Medical Association (Declaration of Helsinki). Alaerts et al., 2011). To date, two studies investigated the causal relationship General Procedure between the ability to perceive PLDs and intact functioning of the All subjects received tDCS during the completion of a bod- (right) pSTS (Grossman et al., 2005; van Kemenade et al., 2012). In ily emotion recognition task and a control task. They partici- these studies, repetitive transcranial magnetic stimulation (rTMS) pated in two stimulation sessions where tDCS was applied with was used to temporarily disrupt activity in right pSTS and both anodal (excitatory) or cathodal (inhibitory) electrodes mounted reported deteriorated performance on a task involving the detec- over the right posterior superior temporal sulcus (pSTS) (target) tion of biological motion in noise-masked displays (Grossman and left orbito-frontal cortex (reference). Sessions were separated et al., 2005; van Kemenade et al., 2012). by one week to avoid residual effects of previous stimulations Here, we used a transcranial direct current stimulation (tDCS) (Figure 1A). paradigm to investigate whether neural information processing Prior to the first stimulation session, subjects were familiarized can be up- or down-regulated in order to increase or deteriorate with task instructions and were allowed to practice the tasks. After biological motion perception. Development of brain stimulation a 30-min resting period, tDCS was administered while subjects paradigms that can enhance biological motion perception abilities performed alternating blocks of the emotion recognition task and would be of particular interest for neuropsychiatric conditions the control task. Task performance was initiated 5 min after tDCS that have clear implications in social and communicative domains, onset and lasted 8.5 min. TDCS was presented for 20 min to ensure such as autism spectrum disorders (ASD). At the behavioral level, that it was applied during the entire duration of the tasks. Half ASD-related deficiencies in biological motion perception have of the participants received anodal stimulation