Coordinated control of eye and hand movements in dynamic reaching.

In the present study, we integrated two recent, at first sight contradictory findings regarding the question whether saccadic eye movements can be generated to a newly presented target during an ongoing hand movement. Saccades were measured during so-called adaptive and sustained pointing conditions. In the adapted pointing condition, subjects had to direct both their gaze and arm movements to a displaced target location. The results showed that the eyes could fixate the new target during pointing. In addition, a temporal coupling of these corrective saccades was found with changes in arm movement trajectories when reaching to the new target. In the sustained pointing condition, however, the same subjects had to point to the initial target, while trying to deviate their gaze to a new target that appeared during pointing. It was found that the eyes could not fixate the new target before the hand reached the initial target location. Together, the results indicate that ocular gaze is always forced to follow the target intended by a manual arm movement. A neural mechanism is proposed that couples ocular gaze to the target of an arm movement. Specifically, the mechanism includes a reach neuron layer besides the well-known saccadic layer in the primate superior colliculus. Such a tight, sub-cortical coupling of ocular gaze to the target of a reaching movement can explain the contrasting behavior of the eyes in dependency of whether the eye and hand share the same target position or attempt to move to different locations.

[1]  Sabine Dannenberg,et al.  Arm-movement-related neurons in the primate superior colliculus and underlying reticular formation: comparison of neuronal activity with EMGs of muscles of the shoulder, arm and trunk during reaching , 1997, Experimental Brain Research.

[2]  R. Wurtz,et al.  Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. , 1993, Journal of neurophysiology.

[3]  K. Hoffmann,et al.  Influence of arm movements on saccades in humans , 2000, The European journal of neuroscience.

[4]  John H. R. Maunsell,et al.  The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. , 1987, Journal of neurophysiology.

[5]  H. Bekkering,et al.  Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. , 2001, Journal of neurophysiology.

[6]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[7]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[8]  R. Wurtz,et al.  Interaction of the frontal eye field and superior colliculus for saccade generation. , 2001, Journal of neurophysiology.

[9]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[10]  J Tanji,et al.  Multiple cortical motor areas and temporal sequencing of movements. , 1996, Brain research. Cognitive brain research.

[11]  R. Wurtz,et al.  Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. , 2000, Journal of neurophysiology.

[12]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[13]  M. Goldberg,et al.  Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade. , 2000, Journal of neurophysiology.

[14]  D. Sparks The brainstem control of saccadic eye movements , 2002, Nature Reviews Neuroscience.

[15]  C. Erkelens,et al.  Coordination of hand movements and saccades: evidence for a common and a separate pathway , 2004, Experimental Brain Research.

[16]  R. Wurtz,et al.  Frontal eye field neurons orthodromically activated from the superior colliculus. , 1998, Journal of neurophysiology.

[17]  J. L. Conway,et al.  Deficits in eye movements following frontal eye-field and superior colliculus ablations. , 1980, Journal of neurophysiology.

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

[19]  A. S. Ramoa,et al.  Intrinsic circuitry of the superior colliculus: pharmacophysiological identification of horizontally oriented inhibitory interneurons. , 1998, Journal of neurophysiology.

[20]  C. Prablanc,et al.  Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement , 1986, Nature.

[21]  S. Gielen,et al.  A quantitative analysis of generation of saccadic eye movements by burst neurons. , 1981, Journal of neurophysiology.

[22]  K. Hoffmann,et al.  Anatomical distribution of arm-movement-related neurons in the primate superior colliculus and underlying reticular formation in comparison with visual and saccadic cells , 1997, Experimental Brain Research.

[23]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[24]  R. Wurtz,et al.  Superior Colliculus Cell Responses Related to Eye Movements in Awake Monkeys , 1971, Science.

[25]  J Tanji,et al.  Visually guided saccade versus eye-hand reach: contrasting neuronal activity in the cortical supplementary and frontal eye fields. , 1996, Journal of neurophysiology.

[26]  Lina L. E. Massone,et al.  Local dynamic interactions in the collicular motor map: a neural network model , 1995 .

[27]  Lina L. E. Massone,et al.  A neural-network system for control of eye movements: basic mechanisms , 1994, Biological Cybernetics.

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

[29]  K. Hoffmann,et al.  Correlation of primate superior colliculus and reticular formation discharge with proximal limb muscle activity. , 1999, Journal of neurophysiology.

[30]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. , 1983, Journal of neurophysiology.

[31]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. 3. Cells discharging before eye movements. , 1972, Journal of neurophysiology.

[32]  D L Sparks,et al.  Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. , 1986, Physiological reviews.

[33]  M. Goldberg,et al.  Oculocentric spatial representation in parietal cortex. , 1995, Cerebral cortex.

[34]  K. Hoffmann,et al.  Neurons in the primate superior colliculus coding for arm movements in gaze-related coordinates. , 2000, Journal of neurophysiology.

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

[36]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[37]  J. Schlag,et al.  Unit activity related to spontaneous saccades in frontal dorsomedial cortex of monkey , 2004, Experimental Brain Research.

[38]  M. Goodale,et al.  Visual control of reaching movements without vision of the limb , 2004, Experimental Brain Research.

[39]  R. Douglas,et al.  Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades , 2004, Experimental Brain Research.

[40]  R. Wurtz,et al.  Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. , 1993, Journal of neurophysiology.

[41]  A. Fuchs,et al.  Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. , 2002, Journal of neurophysiology.

[42]  H. Bekkering,et al.  Integration of visual and somatosensory target information in goal-directed eye and arm movements , 1999, Experimental Brain Research.

[43]  Sanjoy Das,et al.  A distributed model of the saccadic system: The effects of internal noise , 1996, Neurocomputing.

[44]  M. Goodale,et al.  Visual control of reaching movements without vision of the limb , 1986, Experimental Brain Research.

[45]  Jennifer A. Mather,et al.  Orienting to Targets by Looking and Pointing: Parallels and Interactions in Ocular and Manual Performance , 1985 .

[46]  Hilbert J. Kappen,et al.  A two-dimensional ensemble coding model for spatial-temporal transformation of saccades in monkey superior colliculus , 1993 .

[47]  R. M. Siegel,et al.  Neurons of area 7 activated by both visual stimuli and oculomotor behavior , 2004, Experimental Brain Research.

[48]  Jos J. Adam,et al.  Interference between saccadic eye and goal-directed hand movements , 2004, Experimental Brain Research.

[49]  W. Fries Inputs from motor and premotor cortex to the superior colliculus of the macaque monkey , 1985, Behavioural Brain Research.

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

[51]  C. C. A. M. Gielen,et al.  Coordination of fast eye and arm movements in a tracking task , 2004, Experimental Brain Research.

[52]  W. Fries Cortical projections to the superior colliculus in the macaque monkey: A retrograde study using horseradish peroxidase , 1984, The Journal of comparative neurology.

[53]  G. Magenes,et al.  Eye-head-hand coordination in pointing at visual targets: spatial and temporal analysis , 2004, Experimental Brain Research.

[54]  P. Schiller,et al.  Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. , 1971, Journal of neurophysiology.