A model for biological motion detection based on motor prediction in the dorsal premotor area

Recent findings regarding dorsal premotor area (PMd) activation during observation of smooth biological movements suggest that this motor-related area detects biological motions. We hypothesize that a neural network in the PMd acquires an invariance of self-induced motor commands for smooth movements and interprets the observed biological motions as ones satisfying the invariance in self-movements. To verify our hypothesis, we developed a recurrent neural network (RNN) to be trained with smooth motor movements, and examined how the RNN acquires biological invariance. The results showed that predictive learning of the RNN contributed to invariance acquisition, which enabled it to detect biological motions. Our findings agree with the fact that the PMd originally functions as a motor predictor. Moreover, this RNN could judge the ankle and wrist trajectories of a walking human as biological regardless of the subject's sex and emotional state.

[1]  D. Yves von Cramon,et al.  Understanding non-biological dynamics with your own premotor system , 2007, NeuroImage.

[2]  P. Viviani,et al.  The law relating the kinematic and figural aspects of drawing movements. , 1983, Acta psychologica.

[3]  Jonathan D. Nelson,et al.  Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery , 2007, NeuroImage.

[4]  John F. Kalaska,et al.  Neural correlates of mental rehearsal in dorsal premotor cortex , 2004, Nature.

[5]  S. Blakemore,et al.  Atypical basic movement kinematics in autism spectrum conditions , 2013, Brain : a journal of neurology.

[6]  J. Cutting,et al.  Temporal and spatial factors in gait perception that influence gender recognition , 1978, Perception & psychophysics.

[7]  A. Young,et al.  Emotion Perception from Dynamic and Static Body Expressions in Point-Light and Full-Light Displays , 2004, Perception.

[8]  A B Schwartz,et al.  Direct cortical representation of drawing. , 1994, Science.

[9]  Talma Hendler,et al.  Neural representations of kinematic laws of motion: Evidence for action-perception coupling , 2007, Proceedings of the National Academy of Sciences.

[10]  Lara Bardi,et al.  Biological motion preference in humans at birth: role of dynamic and configural properties. , 2011, Developmental science.

[11]  C. Von Hofsten Structuring of early reaching movements: a longitudinal study. , 1991, Journal of motor behavior.

[12]  Cinzia Di Dio,et al.  The neural correlates of velocity processing during the observation of a biological effector in the parietal and premotor cortex , 2013, NeuroImage.

[13]  U. Castiello,et al.  Evidence of early development of action planning in the human foetus: a kinematic study , 2006, Experimental Brain Research.

[14]  T. Flash,et al.  Minimum-jerk, two-thirds power law, and isochrony: converging approaches to movement planning. , 1995, Journal of experimental psychology. Human perception and performance.

[15]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[16]  P Viviani,et al.  The Relationship between Curvature and Velocity in Two-Dimensional Smooth Pursuit Eye Movements , 1997, The Journal of Neuroscience.

[17]  F. Simion,et al.  A predisposition for biological motion in the newborn baby , 2008, Proceedings of the National Academy of Sciences.

[18]  Ryo Saegusa,et al.  Nonlinear principal component analysis to preserve the order of principal components , 2003, Neurocomputing.

[19]  N. F. Troje,et al.  2.13 – Biological Motion Perception , 2008 .

[20]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[21]  T. Flash,et al.  The coordination of arm movements: an experimentally confirmed mathematical model , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  Jody C. Culham,et al.  fMRI Activation during Observation of Others' Reach Errors , 2010, Journal of Cognitive Neuroscience.

[23]  Peter Ford Dominey,et al.  Neural network processing of natural language: II. Towards a unified model of corticostriatal function in learning sentence comprehension and non-linguistic sequencing , 2009, Brain and Language.

[24]  Yasmin L. Hashambhoy,et al.  Neural Correlates of Reach Errors , 2005, The Journal of Neuroscience.

[25]  C. Hofsten,et al.  Structuring of early reaching movements: a longitudinal study. , 1991 .

[26]  Dorita H. F. Chang,et al.  Perception of animacy and direction from local biological motion signals. , 2008, Journal of vision.

[27]  Christian Graff,et al.  Four-Day-Old Human Neonates Look Longer at Non-Biological Motions of a Single Point-of-Light , 2007, PloS one.

[28]  Garrison W. Cottrell,et al.  Image compression by back-propagation: An example of extensional programming , 1988 .

[29]  T. Flash,et al.  Neuronal encoding of human kinematic invariants during action observation. , 2010, Cerebral cortex.

[30]  Dorita H. F. Chang,et al.  Characterizing global and local mechanisms in biological motion perception. , 2009, Journal of vision.

[31]  Ravi S. Menon,et al.  Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas , 2003, Experimental Brain Research.

[32]  Mitsuo Kawato,et al.  Acquisition of internal representation by multilayered perceptrons , 1991 .

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

[34]  F. Pollick,et al.  A motion capture library for the study of identity, gender, and emotion perception from biological motion , 2006, Behavior research methods.

[35]  Anne Springer,et al.  Predicting and memorizing observed action: Differential premotor cortex involvement , 2011, Human brain mapping.

[36]  A. Barto,et al.  Distributed motor commands in the limb premotor network , 1993, Trends in Neurosciences.

[37]  Tetsuo Sawaragi,et al.  Self-reflective segmentation of human bodily motions using recurrent neural networks , 2003, IEEE Trans. Ind. Electron..

[38]  R. Schubotz Prediction of external events with our motor system: towards a new framework , 2007, Trends in Cognitive Sciences.

[39]  Paul B. Johnson,et al.  Making arm movements within different parts of space: dynamic aspects in the primate motor cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.