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Links to Social Cognition and Motor Imagery ⇑ Luke E

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Links to Social Cognition and Motor Imagery ⇑ Luke E Cognition 128 (2013) 140–148 Contents lists available at SciVerse ScienceDirect Cognition journal homepage: www.elsevier.com/locate/COGNIT Individual differences in the perception of biological motion: Links to social cognition and motor imagery ⇑ Luke E. Miller a, , Ayse P. Saygin a,b a Department of Cognitive Science, University of California, San Diego, USA b Neurosciences Program, University of California, San Diego, USA article info abstract Article history: Biological motion perception is often claimed to support social cognition, and to rely upon Received 16 October 2012 embodied representations and motor imagery. Are people with higher levels of social traits Revised 10 March 2013 or more vivid motor imagery better at biological motion perception? We administered four Accepted 25 March 2013 experiments measuring sensitivity in using (global) form and (local) motion cues in biolog- ical motion, plus well-established measures of social cognition (e.g., empathy) and motor imagery (e.g., kinesthetic motor imagery). This first systematic investigation of individual Keywords: variability in biological motion processing demonstrated significant relationships between Individual differences these domains, along with a dissociation. Sensitivity for using form cues in biological Biological motion Social cognition motion processing was correlated with social (and not the imagery) measures; sensitivity Motor imagery for using motion cues was correlated with motor imagery (and not the social) measures. These results could not be explained by performance on non-biological control stimuli. We thus show that although both social cognition and motor imagery predict sensitivity to biological motion, these skills likely tap into different aspects of perception. Ó 2013 Elsevier B.V. All rights reserved. 1. Introduction There is significant intersubject variability in the sensi- tivity to biological motion, the sources of which have been Detecting and interpreting the movements of others is explored in only a few studies. In stroke patients, deficits in an important problem that the brain must solve to ensure biological motion processing correlate with deficits in face the survival and wellbeing of an organism. The visual sys- processing, but not with motion coherence thresholds tem can extract biological motion information even in sit- (Saygin, 2007). Individual differences in biological motion uations where other visual cues are impoverished. Point- detection in noise do not correlate with performance on light biological motion stimuli are animations composed other visual tasks involving grouping and segmentation solely of points of light attached to the joints of a moving (Jung, Zabood, Lee, & Blake, 2012). However, this ability agent (Johansson, 1973). When in motion, such stimuli is correlated with gray matter volume in the posterior evoke a vivid percept of a human body in action. Point- superior temporal sulcus and ventral premotor cortex (Gi- light stimuli have allowed researchers to thoroughly inves- laie-Dotan, Kanai, Bahrami, Rees, & Saygin, 2013), brain re- tigate the perceptual mechanisms underlying biological gions critical for the perception of biological motion motion perception for several decades (Blake & Shiffrar, (Grossman & Blake, 2002; Pelphrey & Carter, 2008; Saygin, 2007). 2007; Saygin, Wilson, Hagler, Bates, & Sereno, 2004; van Kemenade, Muggleton, Walsh, & Saygin, 2012). The corre- lates of individual variability in biological motion tasks can ⇑ Corresponding author. Address: 9500 Gilman Drive, Department of also extend into more general perceptual and cognitive do- Cognitive Science, University of California San Diego, La Jolla, CA 92093- 0515, USA. Tel.: +1 858 395 7540. mains. For example, performance in biological motion E-mail addresses: [email protected] (L.E. Miller), [email protected]. tasks correlated with some (e.g., Stroop interference) but edu (A.P. Saygin). not all (e.g., orienting, visual search efficiency) tests of 0010-0277/$ - see front matter Ó 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.cognition.2013.03.013 L.E. Miller, A.P. Saygin / Cognition 128 (2013) 140–148 141 attention and executive function (Chandrasekaran, Turner, a point-light walker. In the presence of moonwalkers, the Bulthoff, & Thornton, 2010). facing direction task requires participants to rely heavily Here, we used direction discrimination tasks with on form information since motion is not informative as to point-light walkers and with non-biological control stimuli the direction of facing. Although it is possible to complete to explore individual differences in sensitivity to biological the direction discrimination task with local motion, when motion in relation to two different domains: social percep- half the trials are moonwalkers, motion cues are no longer tual and cognitive abilities, and motor imagery. informative regarding facing direction. Likewise, the walk- The first potential source of variability we considered ing direction task requires participants to rely heavily was individual differences in social cognition. Although pa- upon local motion cues (the movements of the individual pers on biological motion perception commonly motivate dots, or possibly subgroups of dots) since the facing the research by mentioning how important this ability is direction is not informative as to the direction of walking for social functions, the link between these domains has when half the trials contain moonwalkers. Although it is not been sufficiently explored. There is also active discus- conceivable that this task involves some form processing, sion regarding the relationship between social abilities or integration of form and motion (e.g., if we consider a and biological motion processing in clinical populations version of the template-matching model that is sensitive such as Autism Spectrum Conditions (ASC, see Section 4); to motion through the temporal sequence of form-based here we aimed to explore this relationship in the non-clin- snapshots), the brain would still need to override the ical population. straightforward use of form cues, and it is unlikely for this Another potential correlate of variability in biological task to be performed without strong reliance on motion motion perception is motor imagery, the ability to imagine cues. the performance of an action from first or third person, To explore the specificity of effects to biological motion, either visually or kinesthetically (Lotze & Halsband, analogous tasks were also administered with a non-biolog- 2006). According to simulation theory (often linked with ical control stimuli (a point-light shape, see Section 2). the mirror neuron system; Iacoboni & Dapretto, 2006), both biological motion perception and motor imagery in- 2. Methods volve a (partial) internal simulation of the seen or imag- ined action in the viewer’s own motor representations We administered four experiments of motion process- (Jeannerod, 2001). Here we explored motor imagery with ing as well as a number of experimental and question- the rationale that shared resources with biological motion naire-based measures of social cognition and imagery perception may be evidenced by a correlation between the [Empathy Quotient, Autism-Spectrum Quotient, Reading two abilities. the Mind in the Eyes Test, Cambridge Face Memory Test, In the visual system, form and motion are processed in Vividness of Movement Imagery Questionnaire, which con- partially segregated streams, which are dynamically inte- sists of internal, external and kinesthetic imagery]. All par- grated at multiple levels (Kourtzi, Krekelberg, & van Wezel, ticipants reported normal or corrected-to-normal vision 2008). There is active discussion about the relative role of and no history of mental illness, neurological or cognitive (local) motion information vs. (global) form information impairments. Although we tried to have all participants in biological motion processing, and the underlying neural complete all tests, some attrition inevitably occurred due systems (Beintema & Lappe, 2002; Garcia & Grossman, to the multiple sessions required to administer all experi- 2008; Jastorff & Orban, 2009; Lu, 2010; Thompson, Clarke, ments. The experiments were approved by the UCSD IRB Stewart, & Puce, 2005; Thurman, Giese, & Grossman, 2010). and all participants gave informed consent. Results on the direction discrimination task are especially mixed regarding the involvement of form and motion 2.1. Experiment 1: Biological motion facing direction (Bio- mechanisms. Some researchers have argued that the indi- Facing) vidual local motions of the point-light walker’s limbs play an important role in direction discrimination (e.g. Troje & 2.1.1. Participants Westhoff, 2006). Other data highlight the role of form, Sixty-seven adults (15 males) between 18 and 31 years since the direction discrimination task can also be solved of age (mean: 20.8, SD: 1.73) participated in a biological in the absence of local motion cues (Lange & Lappe, motion task. Subsets of these participants also completed 2007). Thus, the direction discrimination task can be the social cognition and mental imagery measures: Empa- solved by using either form or motion cues. Furthermore, thy Quotient (N = 65), Autism Quotient (N = 65), Reading biological motion processing has been found normal in the Mind in the Eyes Test (N = 59), Cambridge Face Mem- both patients who cannot perceive motion (McLeod, Dit- ory Test (N = 63), Vividness of Motor Imagery Question- trich, Driver,
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