Somatosensory target information is used for reaching but not for saccadic eye movements.

For any type of goal-directed hand and eye movement, it is important to determine the position of the target. Though many of these movements are directed toward visual targets, humans also perform movements to targets derived by somatosensory information only, such as proprioceptive (sensory signals about static limb position), kinaesthetic (sensory signals about limb movement), and tactile signals (sensory signals about touch on skin). In this study we investigated how each of these types of somatosensory information influences goal-directed hand and eye movements. Further, we examined whether somatosensory target information has a differential influence on isolated and combined eye-hand movements. Participants performed right-hand reaching, eye, or coordinated eye-hand movements to their left index or middle fingers in the absence of any visual information. We varied somatosensory target information by allowing proprioceptive, proprioceptive-kinaesthetic, proprioceptive-tactile, or proprioceptive-kinaesthetic-tactile information. Reach endpoint precision was poorest when the target was derived by proprioceptive information only, but improved when two different types of input were available. In addition, reach endpoints in conditions with kinaesthetic target information were systematically shifted toward the direction of movement, while static somatosensory information decayed over time and led to systematic undershoots of the reach target location. In contrast to the effect on reaches, somatosensory information did not influence gaze endpoint accuracy or precision. When performing coordinated eye-hand movements reach accuracy and gaze endpoint precision improved, suggesting a bidirectional use of efferent information. We conclude that somatosensory target information influence endpoint control differently for goal-directed hand and eye movements to unseen targets.

[1]  Gunnar Blohm,et al.  Reaching around obstacles accounts for uncertainty in coordinate transformations. , 2020, Journal of neurophysiology.

[2]  Yon Visell,et al.  Proprioceptive Localization of the Fingers: Coarse, Biased, and Context-Sensitive , 2020, IEEE Transactions on Haptics.

[3]  Hiroki Nakamoto,et al.  Predictive eye movements when hitting a bouncing ball. , 2019, Journal of vision.

[4]  Gerome A Manson,et al.  Auditory cues for somatosensory targets invoke visuomotor transformations: Behavioral and electrophysiological evidence , 2019, PloS one.

[5]  Gerome A Manson,et al.  Rapid online corrections for upper limb reaches to perturbed somatosensory targets: evidence for non-visual sensorimotor transformation processes , 2019, Experimental Brain Research.

[6]  Gunnar Blohm,et al.  Neck muscle spindle noise biases reaches in a multisensory integration task. , 2018, Journal of neurophysiology.

[7]  E. Brenner,et al.  Gaze when reaching to grasp a glass. , 2018, Journal of vision.

[8]  Gunnar Blohm,et al.  Vibrotactile information improves proprioceptive reaching target localization , 2018, PloS one.

[9]  Heiner Deubel,et al.  Independent selection of eye and hand targets suggests effector-specific attentional mechanisms , 2018, Scientific Reports.

[10]  R. Andersen,et al.  Lateral intraparietal area (LIP) is largely effector-specific in free-choice decisions , 2018, Scientific Reports.

[11]  M. Longo Hand Posture Modulates Perceived Tactile Distance , 2017, Scientific Reports.

[12]  Katja Fiehler,et al.  Spatial specificity of tactile enhancement during reaching , 2017, Attention, Perception, & Psychophysics.

[13]  Katja Fiehler,et al.  Gaze-centered coding of proprioceptive reach targets after effector movement: Testing the impact of online information, time of movement, and target distance , 2017, PloS one.

[14]  Brian C J Moore,et al.  Blindness enhances auditory obstacle circumvention: Assessing echolocation, sensory substitution, and visual-based navigation , 2017, PloS one.

[15]  Katja Fiehler,et al.  Enhancement and Suppression of Tactile Signals During Reaching , 2017, Journal of experimental psychology. Human perception and performance.

[16]  Jing Chen,et al.  Role of motor execution in the ocular tracking of self-generated movements. , 2016, Journal of neurophysiology.

[17]  K. Fiehler,et al.  Mixed body- and gaze-centered coding of proprioceptive reach targets after effector movement , 2016, Neuropsychologia.

[18]  K. Fiehler,et al.  Kinesthetic information facilitates saccades towards proprioceptive-tactile targets , 2016, Vision Research.

[19]  J. Wann,et al.  Eye and hand movement strategies in older adults during a complex reaching task , 2016, Experimental Brain Research.

[20]  Simon Grant,et al.  Gaze–grasp coordination in obstacle avoidance: differences between binocular and monocular viewing , 2015, Experimental Brain Research.

[21]  Joan López-Moliner,et al.  Why do movements drift in the dark? Passive versus active mechanisms of error accumulation. , 2015, Journal of neurophysiology.

[22]  P. Haggard,et al.  Dynamic Tuning of Tactile Localization to Body Posture , 2015, Current Biology.

[23]  Laurence Mouchnino,et al.  Opposed optimal strategies of weighting somatosensory inputs for planning reaching movements toward visual and proprioceptive targets. , 2014, Journal of neurophysiology.

[24]  Katja Fiehler,et al.  Effector movement triggers gaze-dependent spatial coding of tactile and proprioceptive-tactile reach targets , 2014, Neuropsychologia.

[25]  Eli Brenner,et al.  Proprioception Is Robust under External Forces , 2013, PloS one.

[26]  J. Randall Flanagan,et al.  Waiting for a hand: saccadic reaction time increases in proportion to hand reaction time when reaching under a visuomotor reversal , 2013, Front. Hum. Neurosci..

[27]  Eric A. Yttri,et al.  Lesions of cortical area LIP affect reach onset only when the reach is accompanied by a saccade, revealing an active eye–hand coordination circuit , 2013, Proceedings of the National Academy of Sciences.

[28]  Katja Fiehler,et al.  Reach endpoint errors do not vary with movement path of the proprioceptive target. , 2012, Journal of neurophysiology.

[29]  Christopher A. Buneo,et al.  The Proprioceptive Map of the Arm Is Systematic and Stable, but Idiosyncratic , 2011, PloS one.

[30]  Eli Brenner,et al.  Reweighting visual cues by touch. , 2011, Journal of vision.

[31]  Katja Fiehler,et al.  Testing the limits of optimal integration of visual and proprioceptive information of path trajectory , 2011, Experimental Brain Research.

[32]  Karl R Gegenfurtner,et al.  Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion. , 2011, Journal of neurophysiology.

[33]  P. Cavanagh,et al.  Predictive remapping of attention across eye movements , 2011, Nature Neuroscience.

[34]  B. Edin,et al.  Human Muscle Spindles Act as Forward Sensory Models , 2010, Current Biology.

[35]  Jeroen B. J. Smeets,et al.  Muscular Torque Can Explain Biases in Haptic Length Perception: A Model Study on the Radial-Tangential Illusion , 2010, EuroHaptics.

[36]  Knut Drewing,et al.  Optimal integration of visual and proprioceptive movement information for the perception of trajectory geometry , 2010, Experimental Brain Research.

[37]  C. Galletti,et al.  Contribution of visual and proprioceptive information to the precision of reaching movements , 2010, Experimental Brain Research.

[38]  S. Gandevia,et al.  The kinaesthetic senses , 2009, The Journal of physiology.

[39]  Philip N. Sabes,et al.  Sensory transformations and the use of multiple reference frames for reach planning , 2009, Nature Neuroscience.

[40]  B. Edin,et al.  Discharges in Human Muscle Receptor Afferents during Block Grasping , 2008, The Journal of Neuroscience.

[41]  R. Johansson,et al.  Gaze behavior when reaching to remembered targets. , 2008, Journal of neurophysiology.

[42]  S. Soto-Faraco,et al.  Changing Reference Frames during the Encoding of Tactile Events , 2008, Current Biology.

[43]  J D Crawford,et al.  Proprioceptive guidance of saccades in eye-hand coordination. , 2006, Journal of neurophysiology.

[44]  J. Wann,et al.  How active gaze informs the hand in sequential pointing movements , 2006, Experimental Brain Research.

[45]  R. Shadmehr,et al.  Why Does the Brain Predict Sensory Consequences of Oculomotor Commands? Optimal Integration of the Predicted and the Actual Sensory Feedback , 2006, The Journal of Neuroscience.

[46]  T. Vilis,et al.  Directional selectivity of BOLD activity in human posterior parietal cortex for memory-guided double-step saccades. , 2006, Journal of neurophysiology.

[47]  S. Gandevia,et al.  Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. , 2005, Journal of neurophysiology.

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

[49]  H Bekkering,et al.  Coordinated control of eye and hand movements in dynamic reaching. , 2002, Human movement science.

[50]  Chris Rorden,et al.  Enhanced Tactile Performance at the Destination of an Upcoming Saccade , 2002, Current Biology.

[51]  Stefan Everling,et al.  Hand-eye coordination for rapid pointing movements , 2002, Experimental Brain Research.

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

[53]  Christopher A. Buneo,et al.  Direct visuomotor transformations for reaching , 2002, Nature.

[54]  A. Pouget,et al.  Multisensory spatial representations in eye-centered coordinates for reaching , 2002, Cognition.

[55]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[56]  O. Blanke,et al.  Saccades guided by somatosensory stimuli , 2001, Vision Research.

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

[58]  H. Bekkering,et al.  Ocular gaze is anchored to the target of an ongoing pointing movement. , 2000, Journal of neurophysiology.

[59]  R. J. van Beers,et al.  Integration of proprioceptive and visual position-information: An experimentally supported model. , 1999, Journal of neurophysiology.

[60]  M. Land,et al.  The Roles of Vision and Eye Movements in the Control of Activities of Daily Living , 1998, Perception.

[61]  Jean-Louis Vercher,et al.  Manuo-ocular coordination in target tracking. I. A model simulating human performance , 1997, Biological Cybernetics.

[62]  Daniel M. Wolpert,et al.  Forward Models for Physiological Motor Control , 1996, Neural Networks.

[63]  Yiannis Aloimonos,et al.  Vision and action , 1995, Image Vis. Comput..

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

[65]  C. Prablanc,et al.  Automatic control during hand reaching at undetected two-dimensional target displacements. , 1992, Journal of neurophysiology.

[66]  J. F. Soechting,et al.  Errors in pointing are due to approximations in sensorimotor transformations. , 1989, Journal of neurophysiology.

[67]  Otmar Bock,et al.  Coordination of arm and eye movements in tracking of sinusoidally moving targets , 1987, Behavioural Brain Research.

[68]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[69]  Katja Fiehler,et al.  Saccades and reaches curve away from the other effector's target in simultaneous eye and hand movements. , 2018, Journal of neurophysiology.

[70]  Jos J. Adam,et al.  Reaction time latencies of eye and hand movements in single- and dual-task conditions , 2004, Experimental Brain Research.

[71]  C. C. A. M. Gielen,et al.  The attainment of target position during step-tracking movements despite a shift of initial position , 2004, Experimental Brain Research.

[72]  Mary M Hayhoe,et al.  Visual memory and motor planning in a natural task. , 2003, Journal of vision.

[73]  D. Sparks,et al.  Saccades to somatosensory targets. I. behavioral characteristics. , 1996, Journal of neurophysiology.

[74]  J. Gordon,et al.  Impairments of reaching movements in patients without proprioception. II. Effects of visual information on accuracy. , 1995, Journal of neurophysiology.