TMS reveals flexible use of form and motion cues in biological motion perception

The perception of human movement is a key component of daily social interactions. Although extrastriate area MT+/V5 is closely associated with motion processing, its role in the processing of sparse 'biological motion' displays is still unclear. We developed two closed matched psychophysical tasks to assess simple coherent motion perception and biological motion perception, and measured changes in performance caused by application of TMS over MT+/V5. Performance of the simple motion discrimination task was significantly depressed by TMS stimulation, and highly correlated within observers in TMS conditions, but there was no significant decrement in performance of the biological motion task, despite low intra-observer correlations across TMS conditions. We conclude that extrastriate area MT+/V5 is an obligatory waypoint in the neural processing of simple coherent motion, but is not obligatory for the processing of biological motion. Results are consistent with a dual neural processing route for biological motion processing.

[1]  C. Umilta,et al.  The use of transcranial magnetic stimulation in cognitive neuroscience: A new synthesis of methodological issues , 2011, Neuroscience & Biobehavioral Reviews.

[2]  Denis Schluppeck,et al.  Temporal characteristics of global motion processing revealed by transcranial magnetic stimulation , 2009, The European journal of neuroscience.

[3]  D. Sheinberg,et al.  Temporal Cortex Neurons Encode Articulated Actions as Slow Sequences of Integrated Poses , 2010, The Journal of Neuroscience.

[4]  B. Bertenthal,et al.  Does Perception of Biological Motion Rely on Specific Brain Regions? , 2001, NeuroImage.

[5]  Aaron R. Seitz,et al.  What a difference a parameter makes: A psychophysical comparison of random dot motion algorithms , 2009, Vision Research.

[6]  V. Walsh,et al.  State-dependency in brain stimulation studies of perception and cognition , 2008, Trends in Cognitive Sciences.

[7]  Juha Silvanto,et al.  The Causal Role of the Occipital Face Area (OFA) and Lateral Occipital (LO) Cortex in Symmetry Perception , 2015, The Journal of Neuroscience.

[8]  Joris Vangeneugden,et al.  Distinct Neural Mechanisms for Body Form and Body Motion Discriminations , 2014, The Journal of Neuroscience.

[9]  Neil G. Muggleton,et al.  New light through old windows: Moving beyond the “virtual lesion” approach to transcranial magnetic stimulation , 2008, NeuroImage.

[10]  M. Thirkettle,et al.  Contributions of form, motion and task to biological motion perception. , 2009, Journal of vision.

[11]  A. Mizuno,et al.  A change of the leading player in flow Visualization technique , 2006, J. Vis..

[12]  Neil G. Muggleton,et al.  Effects of TMS over Premotor and Superior Temporal Cortices on Biological Motion Perception , 2012, Journal of Cognitive Neuroscience.

[13]  G. Mather,et al.  Low-level visual processing of biological motion , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[14]  Jeffrey N. Rouder,et al.  Bayesian t tests for accepting and rejecting the null hypothesis , 2009, Psychonomic bulletin & review.

[15]  Geraint Rees,et al.  Ventral aspect of the visual form pathway is not critical for the perception of biological motion , 2015, Proceedings of the National Academy of Sciences.

[16]  Lucia M. Vaina,et al.  The role of human extra-striate visual areas V5/MT and V2/V3 in the perception of the direction of global motion: a transcranial magnetic stimulation study , 2006, Experimental Brain Research.

[17]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[18]  N. Troje,et al.  The Inversion Effect in Biological Motion Perception: Evidence for a “Life Detector”? , 2006, Current Biology.

[19]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[20]  Juha Silvanto,et al.  Transcranial magnetic stimulation reveals the content of visual short-term memory in the visual cortex , 2010, NeuroImage.

[21]  V. Hömberg,et al.  Cerebral visual motion blindness: transitory akinetopsia induced by transcranial magnetic stimulation of human area V5 , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  I. Thornton The visual perception of human locomotion. , 1998, Cognitive neuropsychology.

[23]  Jeffrey N. Rouder,et al.  Bayes factor approaches for testing interval null hypotheses. , 2011, Psychological methods.

[24]  Gianluca Campana,et al.  The fastest (and simplest), the earliest: The locus of processing of rapid forms of motion aftereffect , 2011, Neuropsychologia.

[25]  Steven M. Thurman,et al.  Perceptual and computational analysis of critical features for biological motion. , 2010, Journal of vision.

[26]  J. Bullier,et al.  Anatomical segregation of two cortical visual pathways in the macaque monkey , 1990, Visual Neuroscience.

[27]  Justin A. Harris,et al.  Neuroscience and Biobehavioral Reviews Modelling Non-invasive Brain Stimulation in Cognitive Neuroscience , 2022 .

[28]  R. Blake,et al.  Brain Areas Involved in Perception of Biological Motion , 2000, Journal of Cognitive Neuroscience.

[29]  J A Beintema,et al.  Perception of biological motion without local image motion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[31]  Lisa Koski,et al.  A double dissociation between striate and extrastriate visual cortex for pattern motion perception revealed using rTMS , 2009, Human brain mapping.

[32]  Á. Pascual-Leone,et al.  Repetitive TMS over posterior STS disrupts perception of biological motion , 2005, Vision Research.

[33]  Gianluca Campana,et al.  Priming of motion direction and area V5/MT: a test of perceptual memory. , 2002, Cerebral cortex.

[34]  Rainer Goebel,et al.  The temporal characteristics of motion processing in hMT/V5+: Combining fMRI and neuronavigated TMS , 2006, NeuroImage.

[35]  M. Lappe,et al.  Perception of biological motion from limited-lifetime stimuli , 2006, Perception & psychophysics.

[36]  Juha Silvanto,et al.  Making the blindsighted see , 2007, Neuropsychologia.

[37]  J E Cutting,et al.  A biomechanical invariant for gait perception. , 1978, Journal of experimental psychology. Human perception and performance.