Visual and Tactile Guidance of Dexterous Manipulation Tasks: An fMRI Study

Models of motor guidance that dynamically adjust to the availability and quality of sensory information are based on the observation that dexterous tasks are routinely performed using various combinations of visual and tactile inputs. However, a dynamic neural system that acquires and processes relevant visual and tactile information remains relatively uncharacterized in humans. In this study, whole-brain functional magnetic resonance images were acquired during a dexterous manipulation task, compression of the end caps of a slender spring prone to buckling, to investigate the neural systems associated with motor guidance under four visual and tactile guidance conditions: (1) eyes closed (no visual input), smooth end caps, (2) eyes closed, rough end caps, (3) eyes open and watching hand, smooth end caps, and (4) eyes open and watching hand, rough end caps. Performance of the dexterous task remained constant in all conditions. Variations in the two levels of visual input resulted in modulation of activity in the middle and inferior occipital gyrii and inferior parietal lobule, and variation in the two levels of tactile input during the task resulted in modulation of activity in the precentral (primary motor) gyrus. Although significantly active in all conditions, cingulate gyrus, medial frontal gyrus, postcentral gyrus, and cerebellum activities were not modulated by levels of either visual or somatosensory input, and no interaction effects were observed. Together, these data indicate that a fine-tuned motor task guided by varying visual and tactile information engages a distributed and integrated neural complex consisting of control and executive functions and regions that process dynamic sensory information related to guidance functions.

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

[2]  Leslie G. Ungerleider,et al.  Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys , 1982, Behavioural Brain Research.

[3]  G Meyer,et al.  Forms and spatial arrangement of neurons in the primary motor cortex of man , 1987, The Journal of comparative neurology.

[4]  G. Rizzolatti,et al.  Thalamic input to inferior area 6 and area 4 in the macaque monkey , 1989, The Journal of comparative neurology.

[5]  S. Ogawa,et al.  Oxygenation‐sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields , 1990, Magnetic resonance in medicine.

[6]  Leslie G. Ungerleider,et al.  Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque , 1990, The Journal of comparative neurology.

[7]  C. Darian‐Smith,et al.  Thalamic projections to sensorimotor cortex in the macaque monkey: Use of multiple retrograde fluorescent tracers , 1990, The Journal of comparative neurology.

[8]  P A Salin,et al.  Visual activity in areas V3a and V3 during reversible inactivation of area V1 in the macaque monkey. , 1991, Journal of neurophysiology.

[9]  J. Mazziotta,et al.  MRI‐PET Registration with Automated Algorithm , 1993, Journal of computer assisted tomography.

[10]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  A. Patla,et al.  Waterloo Vision and Mobility Study: gait adaptations to altered surfaces in individuals with age-related maculopathy. , 1994, Optometry and vision science : official publication of the American Academy of Optometry.

[12]  R S Johansson,et al.  Grasp stability during manipulative actions. , 1994, Canadian journal of physiology and pharmacology.

[13]  J. Gordon,et al.  Learning a visuomotor transformation in a local area of work space produces directional biases in other areas. , 1995, Journal of neurophysiology.

[14]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[15]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[16]  Michael I. Jordan,et al.  Generalization to Local Remappings of the Visuomotor Coordinate Transformation , 1996, The Journal of Neuroscience.

[17]  Paul B. Johnson,et al.  The sources of visual information to the primate frontal lobe: a novel role for the superior parietal lobule. , 1996, Cerebral cortex.

[18]  P J Sparto,et al.  Effect of aging on human postural control during cognitive tasks. , 1997, Biomedical sciences instrumentation.

[19]  P. Strick,et al.  Motor areas on the medial wall of the hemisphere. , 1998, Novartis Foundation symposium.

[20]  M Kawato,et al.  Internal models for motor control. , 2007, Novartis Foundation symposium.

[21]  F. Zajac,et al.  Large index-fingertip forces are produced by subject-independent patterns of muscle excitation. , 1998, Journal of biomechanics.

[22]  K. J. Cole,et al.  Tactile impairments cannot explain the effect of age on a grasp and lift task , 1998, Experimental Brain Research.

[23]  R. J. Seitz,et al.  A fronto‐parietal circuit for object manipulation in man: evidence from an fMRI‐study , 1999, The European journal of neuroscience.

[24]  John W. Krakauer,et al.  Independent learning of internal models for kinematic and dynamic control of reaching , 1999, Nature Neuroscience.

[25]  J B Poline,et al.  Transient Activity in the Human Calcarine Cortex During Visual-Mental Imagery: An Event-Related fMRI Study , 2000, Journal of Cognitive Neuroscience.

[26]  F. Valero-Cuevas Predictive modulation of muscle coordination pattern magnitude scales fingertip force magnitude over the voluntary range. , 2000, Journal of neurophysiology.

[27]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[28]  D. Heeger,et al.  Activity in primary visual cortex predicts performance in a visual detection task , 2000, Nature Neuroscience.

[29]  J. Hirsch,et al.  An Integrated Functional Magnetic Resonance Imaging Procedure for Preoperative Mapping of Cortical Areas Associated with Tactile, Motor, Language, and Visual Functions , 2000, Neurosurgery.

[30]  R. Johansson,et al.  Cortical activity in precision- versus power-grip tasks: an fMRI study. , 2000, Journal of neurophysiology.

[31]  P. Matthews,et al.  Functional MRI cerebral activation and deactivation during finger movement , 2000, Neurology.

[32]  N Vuillerme,et al.  The effect of expertise in gymnastics on proprioceptive sensory integration in human subjects , 2001, Neuroscience Letters.

[33]  F. Lacquaniti,et al.  Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. , 2001, Cerebral cortex.

[34]  C D Davlin,et al.  The role of vision in control of orientation in a back tuck somersault. , 2001, Motor control.

[35]  L Krubitzer,et al.  Thalamo‐cortical connections of areas 3a and M1 in marmoset monkeys , 2001, The Journal of comparative neurology.

[36]  J. Rauschecker,et al.  Hierarchical Organization of the Human Auditory Cortex Revealed by Functional Magnetic Resonance Imaging , 2001, Journal of Cognitive Neuroscience.

[37]  H. Forssberg,et al.  Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. , 2001, Journal of neurophysiology.

[38]  M. Bonnard,et al.  Interaction between different sensory cues in the control of human gait , 2002, Experimental Brain Research.

[39]  Joy Hirsch,et al.  Interconnected Large-Scale Systems for Three Fundamental Cognitive Tasks Revealed by Functional MRI , 2001, Journal of Cognitive Neuroscience.

[40]  D Elliott,et al.  Specificity versus variability: effects of practice conditions on the use of afferent information for manual aiming. , 2001, Motor control.

[41]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[42]  Hans Forssberg,et al.  Human brain activity in the control of fine static precision grip forces: an fMRI study , 2001, The European journal of neuroscience.

[43]  Ravi S. Menon,et al.  Differential Effects of Viewpoint on Object-Driven Activation in Dorsal and Ventral Streams , 2002, Neuron.

[44]  Anthony R. Dickinson,et al.  Non-spatial, motor-specific activation in posterior parietal cortex , 2002, Nature Neuroscience.

[45]  Stephen M. Kosslyn,et al.  Visual cortex excitability increases during visual mental imagery—a TMS study in healthy human subjects , 2002, Brain Research.

[46]  S. Kiebel,et al.  Visuomotor control within a distributed parieto-frontal network , 2002, Experimental Brain Research.

[47]  Arthur D Kuo,et al.  The relative roles of feedforward and feedback in the control of rhythmic movements. , 2002, Motor control.

[48]  F. Valero-Cuevas,et al.  The strength-dexterity test as a measure of dynamic pinch performance. , 2003, Journal of biomechanics.

[49]  R. Johansson,et al.  Evidence for the involvement of the posterior parietal cortex in coordination of fingertip forces for grasp stability in manipulation. , 2003, Journal of neurophysiology.

[50]  M. Kawato,et al.  Coordinates transformation and learning control for visually-guided voluntary movement with iteration: A Newton-like method in a function space , 1988, Biological Cybernetics.

[51]  H. Asanuma,et al.  Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey , 2004, Experimental Brain Research.

[52]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.