Inducing any virtual two-dimensional movement in humans by applying muscle tendon vibration.

In humans, tendon vibration evokes illusory sensation of movement. We developed a model mimicking the muscle afferent patterns corresponding to any two-dimensional movement and checked its validity by inducing writing illusory movements through specific sets of muscle vibrators. Three kinds of illusory movements were compared. The first was induced by vibration patterns copying the responses of muscle spindle afferents previously recorded by microneurography during imposed ankle movements. The two others were generated by the model. Sixteen different vibratory patterns were applied to 20 motionless volunteers in the absence of vision. After each vibration sequence, the participants were asked to name the corresponding graphic symbol and then to reproduce the illusory movement perceived. Results showed that the afferent patterns generated by the model were very similar to those recorded microneurographically during actual ankle movements (r=0.82). The model was also very efficient for generating afferent response patterns at the wrist level, if the preferred sensory directions of the wrist muscle groups were first specified. Using recorded and modeled proprioceptive patterns to pilot sets of vibrators placed at the ankle or wrist levels evoked similar illusory movements, which were correctly identified by the participants in three quarters of the trials. Our proprioceptive model, based on neurosensory data recorded in behaving humans, should then be a useful tool in fields of research such as sensorimotor learning, rehabilitation, and virtual reality.

[1]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  B. Edin,et al.  Skin strain patterns provide kinaesthetic information to the human central nervous system. , 1995, The Journal of physiology.

[3]  D. F. Collins,et al.  Movement illusions evoked by ensemble cutaneous input from the dorsum of the human hand. , 1996, The Journal of physiology.

[4]  J. Roll,et al.  Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study , 2004, Experimental Brain Research.

[5]  A. Schwartz Motor cortical activity during drawing movements: single-unit activity during sinusoid tracing. , 1992, Journal of neurophysiology.

[6]  Mikael Bergenheim,et al.  Proprioceptive population coding of two-dimensional limb movements in humans: II. Muscle-spindle feedback during "drawing-like" movements , 2000, Experimental Brain Research.

[7]  Mikael Bergenheim,et al.  Microneurography in Humans , 1999 .

[8]  J. F. Soechting,et al.  Use of tactile afferent information in sequential finger movements , 2004, Experimental Brain Research.

[9]  A. Georgopoulos,et al.  Static spatial effects in motor cortex and area 5: Quantitative relations in a two-dimensional space , 1984, Experimental Brain Research.

[10]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  J. Roll,et al.  Proprioceptive sensory codes mediating movement trajectory perception: human hand vibration-induced drawing illusions. , 1995, Canadian journal of physiology and pharmacology.

[12]  Mikael Bergenheim,et al.  The preferred sensory direction of muscle spindle primary endings influences the velocity coding of two-dimensional limb movements in humans , 2002, Experimental Brain Research.

[13]  D. Burke,et al.  The responses of human muscle spindle endings to vibration of non‐contracting muscles. , 1976, The Journal of physiology.

[14]  Gary C Sieck,et al.  Neural control of movement , 2004 .

[15]  Sabine M P Verschueren,et al.  Position sensitivity of human muscle spindles: single afferent and population representations. , 2002, Journal of neurophysiology.

[16]  E. Ribot-Ciscar,et al.  The Ia afferent feedback of a given movement evokes the illusion of the same movement when returned to the subject via muscle tendon vibration , 2006, Experimental Brain Research.

[17]  P J Cordo,et al.  Kinesthetic control of a multijoint movement sequence. , 1990, Journal of neurophysiology.

[18]  A B Schwartz,et al.  Arm trajectory and representation of movement processing in motor cortical activity , 2000, The European journal of neuroscience.

[19]  Frederic Albert,et al.  Proprioceptive feedback in humans expresses motor invariants during writing , 2005, Experimental Brain Research.

[20]  Jean-Pierre Roll,et al.  Proprioceptive population coding of two-dimensional limb movements in humans: I. Muscle spindle feedback during spatially oriented movements , 2000, Experimental Brain Research.

[21]  D. Burke,et al.  Does the nervous system depend on kinesthetic information to control natural limb movements , 1992 .

[22]  H. Johansson,et al.  Comparison of brain activity during different types of proprioceptive inputs: a positron emission tomography study , 2002, Experimental Brain Research.

[23]  D. McCloskey,et al.  The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. , 1972, Brain : a journal of neurology.

[24]  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.

[25]  E. Ribot-Ciscar,et al.  Cutaneous afferents provide a neuronal population vector that encodes the orientation of human ankle movements , 2007, The Journal of physiology.

[26]  Roll Jp,et al.  Proprioceptive sensory codes mediating movement trajectory perception: human hand vibration-induced drawing illusions. , 1995, Canadian journal of physiology and pharmacology.

[27]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. I. Relations between single cell discharge and direction of movement , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  L. Rowell,et al.  Exercise : regulation and integration of multiple systems , 1996 .

[29]  T. Ebner,et al.  Processing of multiple kinematic signals in the cerebellum and motor cortices , 2000, Brain Research Reviews.

[30]  J. Roll,et al.  Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography , 2004, Experimental Brain Research.

[31]  S. Gandevia Kinesthesia : roles for afferent signals and motor commands , 1996 .

[32]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during sinusoid tracing. , 1993, Journal of neurophysiology.

[33]  Frédéric Albert,et al.  “Proprioceptive signature” of cursive writing in humans: a multi-population coding , 2004, Experimental Brain Research.

[34]  D. Humphrey,et al.  Motor control : concepts and issues , 1991 .

[35]  A B Vallbo,et al.  Directional tuning of human forearm muscle afferents during voluntary wrist movements , 2001, The Journal of physiology.

[36]  E. Gentaz,et al.  The visuo-haptic and haptic exploration of letters increases the kindergarten-children's understanding of the alphabetic principle , 2004 .

[37]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during lemniscate tracing. , 1999, Journal of neurophysiology.

[38]  P. Viviani,et al.  Perceiving and tracking kinesthetic stimuli: further evidence of motor-perceptual interactions. , 1997, Journal of experimental psychology. Human perception and performance.