Visual gravity cues in the interpretation of biological movements: neural correlates in humans

Our visual system takes into account the effects of Earth gravity to interpret biological motion (BM), but the neural substrates of this process remain unclear. Here we measured functional magnetic resonance (fMRI) signals while participants viewed intact or scrambled stick-figure animations of walking, running, hopping, and skipping recorded at normal or reduced gravity. We found that regions sensitive to BM configuration in the occipito-temporal cortex (OTC) were more active for reduced than normal gravity but with intact stimuli only. Effective connectivity analysis suggests that predictive coding of gravity effects underlies BM interpretation. This process might be implemented by a family of snapshot neurons involved in action monitoring.

[1]  Alfonso Caramazza,et al.  Distinct Regions of Right Temporal Cortex Are Associated with Biological and Human–Agent Motion: Functional Magnetic Resonance Imaging and Neuropsychological Evidence , 2013, The Journal of Neuroscience.

[2]  Joris Vangeneugden,et al.  Distinct Mechanisms for Coding of Visual Actions in Macaque Temporal Cortex , 2011, The Journal of Neuroscience.

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

[4]  Francesco Lacquaniti,et al.  Changes of Gait Kinematics in Different Simulators of Reduced Gravity , 2013, Journal of motor behavior.

[5]  Guy A. Orban,et al.  Integration of shape and motion cues in biological motion processing in the monkey STS , 2012, NeuroImage.

[6]  R. Blake,et al.  Brain activity evoked by inverted and imagined biological motion , 2001, Vision Research.

[7]  J. Haxby,et al.  fMRI Responses to Video and Point-Light Displays of Moving Humans and Manipulable Objects , 2003, Journal of Cognitive Neuroscience.

[8]  Roel M. Willems,et al.  Complementary Systems for Understanding Action Intentions , 2008, Current Biology.

[9]  B. Cohen,et al.  Relative contribution of walking velocity and stepping frequency to the neural control of locomotion , 2008, Experimental Brain Research.

[10]  Francesco Lacquaniti,et al.  Contributions of the Human Temporoparietal Junction and MT/V5+ to the Timing of Interception Revealed by Transcranial Magnetic Stimulation , 2008, The Journal of Neuroscience.

[11]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[12]  R. Saxe,et al.  Theory of Mind: A Neural Prediction Problem , 2013, Neuron.

[13]  M. Sereno,et al.  Point-Light Biological Motion Perception Activates Human Premotor Cortex , 2004, The Journal of Neuroscience.

[14]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[15]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[16]  S. Runeson,et al.  Visual perception of lifted weight. , 1981, Journal of experimental psychology. Human perception and performance.

[17]  J. Perner,et al.  Common brain areas engaged in false belief reasoning and visual perspective taking: a meta-analysis of functional brain imaging studies , 2013, Front. Hum. Neurosci..

[18]  G. Orban,et al.  Neural mechanisms of understanding rational actions: middle temporal gyrus activation by contextual violation. , 2011, Cerebral cortex.

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

[20]  Nikolaus F. Troje,et al.  What is biological motion?: Definition, stimuli and paradigms , 2012 .

[21]  Cord Westhoff,et al.  Kinematic cues for person identification from biological motion , 2007, Perception & psychophysics.

[22]  G. Orban,et al.  Human Functional Magnetic Resonance Imaging Reveals Separation and Integration of Shape and Motion Cues in Biological Motion Processing , 2009, The Journal of Neuroscience.

[23]  Mark H Johnson,et al.  Biological Motion: A Perceptual Life Detector? , 2006, Current Biology.

[24]  Jim M. Monti,et al.  Expectation and Surprise Determine Neural Population Responses in the Ventral Visual Stream , 2010, The Journal of Neuroscience.

[25]  Nikolaus F. Troje,et al.  Structural encoding and recognition of biological motion: evidence from event-related potentials and source analysis , 2005, Behavioural Brain Research.

[26]  Alison J. Wiggett,et al.  Patterns of fMRI Activity Dissociate Overlapping Functional Brain Areas that Respond to Biological Motion , 2006, Neuron.

[27]  P. Hluštík,et al.  Effects of spatial smoothing on fMRI group inferences. , 2008, Magnetic resonance imaging.

[28]  Karl J. Friston,et al.  Structural and Functional Brain Networks: From Connections to Cognition , 2013, Science.

[29]  Randolph Blake,et al.  Perception of Biological Motion in Schizophrenia and Healthy Individuals: A Behavioral and fMRI Study , 2011, PloS one.

[30]  Daniel Jokisch,et al.  Biological motion as a cue for the perception of size. , 2003, Journal of vision.

[31]  G. Johansson.  Visual perception of biological motion and a model for its analysis , 1973 .

[32]  Giorgio Vallortigara,et al.  Gravity bias in the interpretation of biological motion by inexperienced chicks , 2006, Current Biology.

[33]  R. Blake,et al.  Perception of human motion. , 2007, Annual review of psychology.

[34]  Luca Passamonti,et al.  Changes in “Top-Down” Connectivity Underlie Repetition Suppression in the Ventral Visual Pathway , 2011, The Journal of Neuroscience.

[35]  J. Lange,et al.  A Model of Biological Motion Perception from Configural Form Cues , 2006, The Journal of Neuroscience.

[36]  Hfd Chang,et al.  Shape-Independent Processing of Biological Motion , 2013 .

[37]  A. Borst.  Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[38]  G. Orban,et al.  Specificity of regions processing biological motion , 2005, The European journal of neuroscience.

[39]  Dorita H. F. Chang,et al.  Body Configuration Modulates the Usage of Local Cues to Direction in Biological-Motion Perception , 2011, Psychological science.

[40]  Alireza Gharabaghi,et al.  Cerebellar engagement in an action observation network. , 2010, Cerebral cortex.

[41]  P. Viviani,et al.  Unfamiliar Walking Movements Are Detected Early in the Visual Stream: An fMRI Study. , 2015, Cerebral cortex.

[42]  F. Lacquaniti,et al.  Representation of Visual Gravitational Motion in the Human Vestibular Cortex , 2005, Science.

[43]  G. Cavagna,et al.  The sources of external work in level walking and running. , 1976, The Journal of physiology.

[44]  Guy Orban,et al.  Processing of targets in smooth or apparent motion along the vertical in the human brain: an fMRI study. , 2010, Journal of neurophysiology.

[45]  N. Birbaumer,et al.  Dissociable cortical processing of recognizable and non-recognizable biological movement: analysing gamma MEG activity. , 2004, Cerebral cortex.

[46]  Bennett I. Bertenthal,et al.  Global Processing of Biological Motions , 1994 .

[47]  T. Shipley.  The Effect of Object and Event Orientation on Perception of Biological Motion , 2003, Psychological science.

[48]  Vincenzo Maffei,et al.  Vestibular nuclei and cerebellum put visual gravitational motion in context. , 2008, Journal of neurophysiology.

[49]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

[50]  F. Lacquaniti,et al.  Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity. , 2002, Journal of neurophysiology.

[51]  J. Haxby,et al.  Parallel Visual Motion Processing Streams for Manipulable Objects and Human Movements , 2002, Neuron.

[52]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

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

[54]  T. Poggio,et al.  Cognitive neuroscience: Neural mechanisms for the recognition of biological movements , 2003, Nature Reviews Neuroscience.

[55]  J. Donelan,et al.  The effect of reduced gravity on the kinematics of human walking: a test of the dynamic similarity hypothesis for locomotion. , 1997, The Journal of experimental biology.

[56]  C. Summerfield,et al.  Expectation (and attention) in visual cognition , 2009, Trends in Cognitive Sciences.

[57]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[58]  Emily S. Cross,et al.  Robotic movement preferentially engages the action observation network , 2012, Human brain mapping.

[59]  M. Lindquist.  The Statistical Analysis of fMRI Data. , 2008, 0906.3662.

[60]  Hakwan Lau,et al.  Prior Expectation Modulates the Interaction between Sensory and Prefrontal Regions in the Human Brain , 2011, The Journal of Neuroscience.

[61]  Lara Bardi,et al.  The first time ever I saw your feet: inversion effect in newborns' sensitivity to biological motion. , 2014, Developmental psychology.

[62]  Francesco Lacquaniti,et al.  Gait transitions in simulated reduced gravity. , 2011, Journal of applied physiology.

[63]  Dorita H. F. Chang,et al.  Frames of reference for biological motion and face perception. , 2010, Journal of vision.

[64]  Karl J. Friston,et al.  Predictive coding: an account of the mirror neuron system , 2007, Cognitive Processing.

[65]  P. Sinha,et al.  Functional neuroanatomy of biological motion perception in humans , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[66]  M. Pavlova,et al.  Orientation specificity in biological motion perception , 2000, Perception & psychophysics.

[67]  Vincenzo Maffei,et al.  Simulated Self-motion in a Visual Gravity Field: Sensitivity to Vertical and Horizontal , 2022 .

[68]  Dorita H. F. Chang,et al.  Acceleration carries the local inversion effect in biological motion perception. , 2009, Journal of vision.

[69]  Anjali Krishnan,et al.  Cluster-extent based thresholding in fMRI analyses: Pitfalls and recommendations , 2014, NeuroImage.

[70]  F. Lacquaniti,et al.  Two-thirds power law in human locomotion: role of ground contact forces , 2002, Neuroreport.

[71]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[72]  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.

[73]  H. Ishiguro,et al.  The thing that should not be: predictive coding and the uncanny valley in perceiving human and humanoid robot actions , 2011, Social cognitive and affective neuroscience.

[74]  S. Sumi.  Upside-down Presentation of the Johansson Moving Light-Spot Pattern , 1984, Perception.