Visual Guidance for Hand Advance but Not Hand Withdrawal in a Reach-to-Eat Task in Adult Humans: Reaching Is a Composite Movement

Many animal species use reaching for food to place in the mouth (reach-to-eat) with a hand, and it may be a primitive movement. Although researchers (I. Q. Whishaw, 2005; A. N. Iwaniuk & I. Q. Whishaw, 2000; M. Gentiluci, I. Toni, S. Chieffi, & G. Pavesi, 1994) have described visual guidance of reaching in both normal and brain-injured human and nonhuman primates, researchers have not described the contribution of vision during advance of the limb to grasp food and during withdrawal of the limb with food to the mouth. To evaluate visual contributions, the authors monitored eye movements in young adults as they reached for food with and without vision. Participants visually engaged the target prior to the 1st hand movement and disengaged it as the food was grasped. Visual occlusion slowed limb advance and altered digit shaping but did not affect withdrawal. The dependence on visual control of advance but not withdrawal suggests that the reach-to-eat movement is a composite of 2 basic movements under visual and tactile/proprioceptive guidance, respectively.

[1]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

[2]  S. Pellis,et al.  Impairment of pronation, supination, and body co-ordination in reach-to-grasp tasks in human Parkinson's disease (PD) reveals homology to deficits in animal models , 2002, Behavioural Brain Research.

[3]  F. Previc.  Functional specialization in the lower and upper visual fields in humans: Its ecological origins and neurophysiological implications , 1990, Behavioral and Brain Sciences.

[4]  Manabu Honda,et al.  Asymmetrical Neural Substrates of Tactile Discrimination in Humans: A Functional Magnetic Resonance Imaging Study , 2004, The Journal of Neuroscience.

[5]  S. A. Wallace,et al.  Temporal constraints in the control of prehensile movement. , 1988, Journal of motor behavior.

[6]  M. Jeannerod.  Visuomotor channels: Their integration in goal-directed prehension , 1999 .

[7]  D Elliott,et al.  Eye-hand coordination in goal-directed aiming. , 2001, Human movement science.

[8]  M. Jeannerod,et al.  Constraints on human arm movement trajectories. , 1987, Canadian journal of psychology.

[9]  M. Jeannerod,et al.  Optimal response of eye and hand motor systems in pointing at a visual target , 1979, Biological Cybernetics.

[10]  Michael A Khan,et al.  Guiding Movements with Internal Representations: A Reach-and-Grasp Task , 2003, Research quarterly for exercise and sport.

[11]  C. Evinger,et al.  Eyelid movements. Mechanisms and normal data. , 1991, Investigative ophthalmology & visual science.

[12]  M. Merzenich,et al.  Representational plasticity in cortical area 3b paralleling tactual-motor skill acquisition in adult monkeys. , 1999, Cerebral cortex.

[13]  Les G. Carlton,et al.  Visual Information: The Control of Aiming Movements , 1981 .

[14]  M. Jeannerod,et al.  The coordination of eye, head, and arm movements during reaching at a single visual target , 2004, Experimental Brain Research.

[15]  Ivan Toni,et al.  Tactile input of the hand and the control of reaching to grasp movements , 1997, Experimental Brain Research.

[16]  S. Vogt,et al.  Vision of the hand and environmental context in human prehension , 2000, Experimental Brain Research.

[17]  Ka-Chun Siu,et al.  Saccadic Output Is Influenced by Limb Kinetics During Eye—Hand Coordination , 2004, Journal of motor behavior.

[18]  H. Bülthoff,et al.  Separate neural pathways for the visual analysis of object shape in perception and prehension , 1994, Current Biology.

[19]  Iwona Stepniewska,et al.  Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J C Rothwell,et al.  Manual motor performance in a deafferented man. , 1982, Brain : a journal of neurology.

[21]  I. Whishaw,et al.  On the origin of skilled forelimb movements , 2000, Trends in Neurosciences.

[22]  I. Whishaw.  How do primates reach , 1994 .

[23]  S. Pellis,et al.  Motor Deficits in Parkinsonian Reaching: Dopa-Sensitivity Influenced by Real-World Task Constraint , 2006, Journal of motor behavior.

[24]  M. Graziano.  The organization of behavioral repertoire in motor cortex. , 2006, Annual review of neuroscience.

[25]  U. Castiello,et al.  Kinematic analysis of the reach to grasp movement in Parkinsons and Huntingtons disease subjects , 1998, Neuropsychologia.

[26]  P. Roland,et al.  Shape and roughness activate different somatosensory areas in the human brain. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Ian Q. Whishaw,et al.  Precision grasps of children and young and old adults: individual differences in digit contact strategy, purchase pattern, and digit posture , 2004, Behavioural Brain Research.

[28]  M. Jeannerod.  The neural and behavioural organization of goal-directed movements , 1990, Psychological Medicine.

[29]  M. Goodale,et al.  Superior performance for visually guided pointing in the lower visual field , 2001, Experimental Brain Research.

[30]  M. Jeannerod.  The timing of natural prehension movements. , 1984, Journal of motor behavior.

[31]  Alain Berthoz,et al.  Contribution of eye positioning to control of the upside-down standing posture , 2004, Experimental Brain Research.

[32]  R J Leigh,et al.  Properties of horizontal saccades accompanied by blinks. , 1998, Journal of neurophysiology.

[33]  S. Pellis,et al.  Pallidal deep brain stimulation and L-dopa do not improve qualitative aspects of skilled reaching in Parkinson's disease , 2005, Behavioural Brain Research.

[34]  S. Jackson,et al.  A Kinematic Analysis of Goal-directed Prehension Movements Executed under Binocular, Monocular, and Memory-guided Viewing Conditions , 1997 .

[35]  A. Wing,et al.  Knowing your nose better than your thumb: measures of over-grasp reveal that face-parts are special for grasping , 2005, Experimental Brain Research.

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

[37]  S. Chieffi,et al.  The role of proprioception in the control of prehension movements: a kinematic study in a peripherally deafferented patient and in normal subjects , 2004, Experimental Brain Research.

[38]  Ian Q. Whishaw,et al.  Changes in the kinematic structure and non-kinematic features of movements during skilled reaching after stroke: A Laban Movement Analysis in two case studies , 2006, Journal of Neuroscience Methods.

[39]  J D Crawford,et al.  Kinematic rules for upper and lower arm contributions to grasp orientation. , 2003, Journal of neurophysiology.

[40]  V. Gullapalli,et al.  Visual Information and Object Size in the Control of Reaching. , 1996, Journal of motor behavior.

[41]  S. Chieffi,et al.  Coordination between the transport and the grasp components during prehension movements , 2004, Experimental Brain Research.

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

[43]  M. Jeannerod,et al.  The coupling of arm and finger movements during prehension , 2004, Experimental Brain Research.

[44]  M. Jeannerod.  Specialized channels for cognitive responses , 1981, Cognition.

[45]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[46]  T. Twitchell.  The automatic grasping responses of infants , 1965 .

[47]  R S Johansson,et al.  Significance of cutaneous input for precise hand movements. , 1985, Electroencephalography and clinical neurophysiology. Supplement.

[48]  J. Paillard,et al.  Static versus Kinetic Visual Cues for the Processing of Spatial Relationships , 1985 .

[49]  Dylan F. Cooke,et al.  Arm movements evoked by electrical stimulation in the motor cortex of monkeys. , 2005, Journal of neurophysiology.

[50]  Anthony R. Dickinson,et al.  Eye-hand coordination: saccades are faster when accompanied by a coordinated arm movement. , 2002, Journal of neurophysiology.