Listening to a walking human activates the temporal biological motion area

A vivid perception of a moving human can be evoked when viewing a few point-lights on the joints of an invisible walker. This special visual ability for biological motion perception has been found to involve the posterior superior temporal sulcus (STSp). However, in everyday life, human motion can also be recognized using acoustic cues. In the present study, we investigated the neural substrate of human motion perception when listening to footsteps, by means of a sparse sampling functional MRI design. We first showed an auditory attentional network that shares frontal and parietal areas previously found in visual attention paradigms. Second, an activation was observed in the auditory cortex (Heschl's gyrus and planum temporale), likely to be related to low-level sound processing. Most strikingly, another activation was evidenced in a STSp region overlapping the temporal biological motion area previously reported using visual input. We thus propose that a part of the STSp region might be a supramodal area involved in human motion recognition, irrespective of the sensory modality input.

[1]  Albert Gjedde,et al.  Separate neural pathways for contour and biological-motion cues in motion-defined animal shapes , 2003, NeuroImage.

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

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

[4]  S. Shipp The brain circuitry of attention , 2004, Trends in Cognitive Sciences.

[5]  Richard S. J. Frackowiak,et al.  Two Modulatory Effects of Attention That Mediate Object Categorization in Human Cortex , 1997, Science.

[6]  Edward T. Bullmore,et al.  A direct demonstration of functional specialization within motion-related visual and auditory cortex of the human brain , 1996, Current Biology.

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

[8]  Geraint Rees,et al.  What can functional imaging reveal about the role of attention in visual awareness? , 2001, Neuropsychologia.

[9]  Régine Kolinsky,et al.  Attention-Dependent Changes of Activation and Connectivity in Dichotic Listening , 2002, NeuroImage.

[10]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[11]  Anne-Lise Giraud,et al.  Distinct functional substrates along the right superior temporal sulcus for the processing of voices , 2004, NeuroImage.

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

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

[14]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[15]  Alan C. Evans,et al.  Specific Involvement of Human Parietal Systems and the Amygdala in the Perception of Biological Motion , 1996, The Journal of Neuroscience.

[16]  B Wicker,et al.  Generalized least-squares method applied to fMRI time series with empirically determined correlation matrix , 2003, NeuroImage.

[17]  D. Pinault The thalamic reticular nucleus: structure, function and concept , 2004, Brain Research Reviews.

[18]  R. Goebel,et al.  Integration of Letters and Speech Sounds in the Human Brain , 2004, Neuron.

[19]  R. Zatorre,et al.  Human temporal-lobe response to vocal sounds. , 2002, Brain research. Cognitive brain research.

[20]  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.

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

[22]  Thierry Chaminade,et al.  Changes of effective connectivity between the lateral and medial parts of the prefrontal cortex during a visual task , 2003, The European journal of neuroscience.

[23]  T. Allison,et al.  Brain Activity Evoked by the Perception of Human Walking: Controlling for Meaningful Coherent Motion , 2003, The Journal of Neuroscience.

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

[25]  Gregory McCarthy,et al.  Polysensory interactions along lateral temporal regions evoked by audiovisual speech. , 2003, Cerebral cortex.

[26]  E. DeYoe,et al.  A comparison of visual and auditory motion processing in human cerebral cortex. , 2000, Cerebral cortex.

[27]  A R Palmer,et al.  Modulation and task effects in auditory processing measured using fMRI , 2000, Human brain mapping.

[28]  Marina Pavlova,et al.  Recruitment of periventricular parietal regions in processing cluttered point-light biological motion. , 2005, Cerebral cortex.

[29]  C. Grady,et al.  “What” and “where” in the human auditory system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Aina Puce,et al.  Electrophysiology and brain imaging of biological motion. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  P. Fonlupt,et al.  A neural network elicited by parametric manipulation of the attention load , 2002, Neuroreport.

[32]  E. Vatikiotis-Bateson,et al.  Perceiving Biological Motion: Dissociating Visible Speech from Walking , 2003, Journal of Cognitive Neuroscience.

[33]  Patrick Cavanagh,et al.  Perception of biological motion in parietal patients , 2003, Neuropsychologia.

[34]  J. Rauschecker,et al.  Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans , 1999, Nature Neuroscience.

[35]  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.

[36]  Jeffrey R Binder,et al.  Human brain regions involved in recognizing environmental sounds. , 2004, Cerebral cortex.

[37]  N. Kanwisher,et al.  Visual attention: Insights from brain imaging , 2000, Nature Reviews Neuroscience.

[38]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[39]  Kazuo Hiraki,et al.  An event-related potentials study of biological motion perception in humans , 2003, Neuroscience Letters.

[40]  T. Griffiths,et al.  Distinct Mechanisms for Processing Spatial Sequences and Pitch Sequences in the Human Auditory Brain , 2003, The Journal of Neuroscience.

[41]  John G. Neuhoff,et al.  Spatiotemporal Pattern of Neural Processing in the Human Auditory Cortex , 2002, Science.

[42]  B. Argall,et al.  Unraveling multisensory integration: patchy organization within human STS multisensory cortex , 2004, Nature Neuroscience.

[43]  David A. Medler,et al.  Neural correlates of sensory and decision processes in auditory object identification , 2004, Nature Neuroscience.

[44]  T. Griffiths,et al.  The planum temporale as a computational hub , 2002, Trends in Neurosciences.

[45]  Alan C. Evans,et al.  A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. , 2000, Cerebral cortex.

[46]  Rieko Osu,et al.  The Neural Substrates of Biological Motion Perception: an fMRI Study , 2022 .

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