The Proprioceptive Map of the Arm Is Systematic and Stable, but Idiosyncratic

Visual and somatosensory signals participate together in providing an estimate of the hand's spatial location. While the ability of subjects to identify the spatial location of their hand based on visual and proprioceptive signals has previously been characterized, relatively few studies have examined in detail the spatial structure of the proprioceptive map of the arm. Here, we reconstructed and analyzed the spatial structure of the estimation errors that resulted when subjects reported the location of their unseen hand across a 2D horizontal workspace. Hand position estimation was mapped under four conditions: with and without tactile feedback, and with the right and left hands. In the task, we moved each subject's hand to one of 100 targets in the workspace while their eyes were closed. Then, we either a) applied tactile stimulation to the fingertip by allowing the index finger to touch the target or b) as a control, hovered the fingertip 2 cm above the target. After returning the hand to a neutral position, subjects opened their eyes to verbally report where their fingertip had been. We measured and analyzed both the direction and magnitude of the resulting estimation errors. Tactile feedback reduced the magnitude of these estimation errors, but did not change their overall structure. In addition, the spatial structure of these errors was idiosyncratic: each subject had a unique pattern of errors that was stable between hands and over time. Finally, we found that at the population level the magnitude of the estimation errors had a characteristic distribution over the workspace: errors were smallest closer to the body. The stability of estimation errors across conditions and time suggests the brain constructs a proprioceptive map that is reliable, even if it is not necessarily accurate. The idiosyncrasy across subjects emphasizes that each individual constructs a map that is unique to their own experiences.

[1]  Robert L. Sainburg,et al.  Lateralization of motor adaptation reveals independence in control of trajectory and steady-state position , 2007, Experimental Brain Research.

[2]  C. Spence Crossmodal spatial attention , 2010, Annals of the New York Academy of Sciences.

[3]  R. Sainburg,et al.  Differences in control of limb dynamics during dominant and nondominant arm reaching. , 2000, Journal of neurophysiology.

[4]  M S Graziano,et al.  Coding the location of the arm by sight. , 2000, Science.

[5]  Astrid M L Kappers,et al.  Large systematic deviations in a bimanual parallelity task: further analysis of contributing factors. , 2003, Acta psychologica.

[6]  J. Wann,et al.  Does limb proprioception drift? , 2004, Experimental Brain Research.

[7]  Jeremy D Wong,et al.  Somatosensory Plasticity and Motor Learning , 2010, The Journal of Neuroscience.

[8]  Nadia Bolognini,et al.  Proprioceptive Alignment of Visual and Somatosensory Maps in the Posterior Parietal Cortex , 2007, Current Biology.

[9]  Michel Desmurget,et al.  Proprioception does not quickly drift during visual occlusion , 2000, Experimental Brain Research.

[10]  P. Haggard,et al.  The brain’s fingers and hands , 2006, Experimental Brain Research.

[11]  Patrick Haggard,et al.  An implicit body representation underlying human position sense , 2010, Proceedings of the National Academy of Sciences.

[12]  J F Soechting,et al.  A coordinate system for the synthesis of visual and kinesthetic information , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  C. Gross,et al.  Visuospatial properties of ventral premotor cortex. , 1997, Journal of neurophysiology.

[14]  C. Spence,et al.  Visuo-tactile links in covert exogenous spatial attention remap across changes in unseen hand posture , 2002, Perception & psychophysics.

[15]  Christopher A. Buneo,et al.  Analyzing neural responses with vector fields , 2011, Journal of Neuroscience Methods.

[16]  J. Lackner,et al.  Motor adaptation to Coriolis force perturbations of reaching movements: endpoint but not trajectory adaptation transfers to the nonexposed arm. , 1995, Journal of neurophysiology.

[17]  D. Goble,et al.  Upper limb asymmetries in the utilization of proprioceptive feedback , 2005, Experimental Brain Research.

[18]  A. Gordon,et al.  Contribution of tactile information to accuracy in pointing movements , 2001, Experimental Brain Research.

[19]  F. Nielsen,et al.  Right temporoparietal cortex activation during visuo-proprioceptive conflict. , 2004, Cerebral Cortex.

[20]  Jonathan D. Cohen,et al.  Rubber hands ‘feel’ touch that eyes see , 1998, Nature.

[21]  Patrick Haggard,et al.  Proprioceptive integration and body representation: insights into dancers’ expertise , 2011, Experimental Brain Research.

[22]  S. Adamovich,et al.  Pointing in 3D space to remembered targets II: Effects of movement speed toward kinesthetically defined targets , 1999, Experimental Brain Research.

[23]  Dylan F. Cooke,et al.  Distribution of hand location in monkeys during spontaneous behavior , 2004, Experimental Brain Research.

[24]  D. Goble,et al.  Upper limb asymmetries in the matching of proprioceptive versus visual targets. , 2008, Journal of neurophysiology.

[25]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[26]  B. Martin,et al.  Position sense asymmetry , 2008, Experimental Brain Research.

[27]  Jeremy D Wong,et al.  Spatially selective enhancement of proprioceptive acuity following motor learning. , 2011, Journal of neurophysiology.

[28]  Proprioceptive deafferentation slows down the processing of visual hand feedback. , 2007, Journal of vision.

[29]  Daniel J. Goble,et al.  Proprioceptive target matching asymmetries in left-handed individuals , 2009, Experimental Brain Research.

[30]  Eli Brenner,et al.  Body-centered visuomotor adaptation. , 2004, Journal of neurophysiology.

[31]  C. Prablanc,et al.  Vectorial coding of movement: vision, proprioception, or both? , 1995, Journal of neurophysiology.

[32]  J. Lackner,et al.  Influences of arm proprioception and degrees of freedom on postural control with light touch feedback. , 2008, Journal of neurophysiology.

[33]  D. Rosenbaum,et al.  Limb position drift: implications for control of posture and movement. , 2003, Journal of neurophysiology.

[34]  Robert L Sainburg,et al.  Handedness: dominant arm advantages in control of limb dynamics. , 2002, Journal of neurophysiology.

[35]  G. Rizzolatti,et al.  Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position , 2004, Experimental Brain Research.

[36]  R. Sainburg,et al.  Differential contributions of vision and proprioception to movement accuracy , 2003, Experimental Brain Research.

[37]  Marco Santello,et al.  Effects of Fusion between Tactile and Proprioceptive Inputs on Tactile Perception , 2011, PloS one.

[38]  P. Haggard,et al.  The Posterior Parietal Cortex Remaps Touch into External Space , 2010, Current Biology.

[39]  J. Lackner,et al.  Fingertip contact suppresses the destabilizing influence of leg muscle vibration. , 2000, Journal of neurophysiology.

[40]  J. Lackner,et al.  Rapid adaptation to Coriolis force perturbations of arm trajectory. , 1994, Journal of neurophysiology.

[41]  J. Lackner,et al.  Aspects of body self-calibration , 2000, Trends in Cognitive Sciences.

[42]  S. Adamovich,et al.  Pointing in 3D space to remembered targets. I. Kinesthetic versus visual target presentation. , 1998, Journal of neurophysiology.

[43]  David A. Rosenbaum,et al.  Movement speed effects on limb position drift , 2003, Experimental Brain Research.

[44]  K. E. Overvliet,et al.  UvA-DARE ( Digital Academic Repository ) Relative finger position influences whether you can localize tactile stimuli , 2010 .

[45]  Ruth Dickstein,et al.  Stance stability with unilateral and bilateral light touch of an external stationary object , 2005, Somatosensory & motor research.

[46]  P. Haggard,et al.  The perceived position of the hand in space , 2000, Perception & psychophysics.

[47]  S. Kitazawa,et al.  Sensation at the tips of invisible tools , 2001, Nature Neuroscience.

[48]  M. Flanders,et al.  Errors in kinesthetic transformations for hand apposition , 1994, Neuroreport.

[49]  Elizabeth T. Wilson,et al.  Mapping Proprioception across a 2D Horizontal Workspace , 2010, PloS one.

[50]  Robert L. Sainburg,et al.  Differential influence of vision and proprioception on control of movement distance , 2006, Experimental Brain Research.

[51]  S. Tillery,et al.  Haptic Interaction of Touch and Proprioception: Implications for Neuroprosthetics , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[52]  Robert L. Sainburg,et al.  Handedness: Differential Specializations for Control of Trajectory and Position , 2005, Exercise and sport sciences reviews.

[53]  Warren G. Darling,et al.  Transformations between visual and kinesthetic coordinate systems in reaches to remembered object locations and orientations , 2004, Experimental Brain Research.

[54]  S. Soto-Faraco,et al.  Alleviating the ‘crossed-hands’ deficit by seeing uncrossed rubber hands , 2007, Experimental Brain Research.

[55]  Francesco Pavani,et al.  Multisensory contributions to the 3-D representation of visuotactile peripersonal space in humans: evidence from the crossmodal congruency task , 2004, Journal of Physiology-Paris.

[56]  Robert J. van Beers,et al.  How humans combine simultaneous proprioceptive and visual position information , 1996, Experimental Brain Research.

[57]  D. Wolpert,et al.  When Feeling Is More Important Than Seeing in Sensorimotor Adaptation , 2002, Current Biology.

[58]  D. Goble,et al.  Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement , 2007, Experimental Brain Research.

[59]  Charles G. Gross,et al.  Visual responses with and without fixation: neurons in premotor cortex encode spatial locations independently of eye position , 1998, Experimental Brain Research.

[60]  Eli Brenner,et al.  Sensory integration does not lead to sensory calibration , 2006, Proceedings of the National Academy of Sciences.

[61]  Anne C. Sittig,et al.  The precision of proprioceptive position sense , 1998, Experimental Brain Research.

[62]  G. Rizzolatti,et al.  Space coding by premotor cortex , 2004, Experimental Brain Research.

[63]  P. Viviani,et al.  Pointing errors reflect biases in the perception of the initial hand position. , 1998, Journal of neurophysiology.

[64]  C. Spence,et al.  Multisensory representation of limb position in human premotor cortex , 2003, Nature Neuroscience.

[65]  James R. Lackner,et al.  The role of haptic cues from rough and slippery surfaces in human postural control , 2004, Experimental Brain Research.

[66]  Motoki Kouzaki,et al.  Reduced postural sway during quiet standing by light touch is due to finger tactile feedback but not mechanical support , 2008, Experimental Brain Research.

[67]  Christina T Fuentes,et al.  Where is your arm? Variations in proprioception across space and tasks. , 2010, Journal of neurophysiology.

[68]  Robert L. Sainburg,et al.  Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy , 2009, Neuropsychologia.

[69]  Ely Rabin,et al.  Influence of fingertip contact on illusory arm movements. , 2004, Journal of applied physiology.

[70]  Robert L. Sainburg,et al.  The dominant and nondominant arms are specialized for stabilizing different features of task performance , 2007, Experimental Brain Research.

[71]  C. Spence,et al.  Multisensory integration and the body schema: close to hand and within reach , 2003, Current Biology.