Abstract
At a descriptive level, prehension movements can be partitioned into three components ensuring, respectively, the transport of the arm to the vicinity of the target, the orientation of the hand according to object tilt, and the grasp itself. Several authors have suggested that this analytic description may be an operational principle for the organization of the motor system. This hypothesis, called “visuomotor channels hypothesis,” is in particular supported by experiments showing a parallelism between the reach and grasp components of prehension movements. The purpose of the present study was to determine whether or not the generalization of the visuomotor channels hypothesis, from its initial form, restricted to the grasp and transport components, to its actual form, including the reach orientation and grasp components, may be well founded. Six subjects were required to reach and grasp cylindrical objects presented at a given location, with different orientations. During the movements, object orientation was either kept constant (unperturbed trials) or modified at movement onset (perturbed trials). Results showed that both wrist path (sequence of positions that the hand follows in space), and wrist trajectory (time sequence of the successive positions of the hand) were strongly affected by object orientation and by the occurrence of perturbations. These observations suggested strongly that arm transport and hand orientation were neither planned nor controlled independently. The significant linear regressions observed, with respect to the time, between arm displacement (integral of the magnitude of the velocity vector) and forearm rotation also supported this view. Interestingly, hand orientation was not implemented at only the distal level, demonstrating that all the redundant degrees of freedom available were used by the motor system to achieve the task. The final configuration reached by the arm was very stable for a given final orientation of the object to grasp. In particular, when object tilt was suddenly modified at movement onset, the correction brought the upper limb into the same posture as that obtained when the object was initially presented along the final orientation reached after perturbation. Taken together, the results described in the present study suggest that arm transport and hand orientation do not constitute independent visuomotor channels. They also further suggest that prehension movements are programmed, from an initial configuration, to reach smoothly a final posture that corresponds to a given “location and orientation” as a whole.
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References
Abend W, Bizzi E, Morasso P (1982) Human arm trajectory formation. Brain 105:331–348
Alstermark B, Lundberg A, Norrrsell U, Sybirska E (1981) Integration in the descending motor pathways controlling the forelimb in the cat. 9. Differential behavioural defects after spinal cord lesion interrupting defined pathways from higher centers to motoneurons. Exp Brain Res 42:287–294
Alstermark B, Gorska T, Lundberg A, Petterson L-G (1990) Integration in the descending motor pathways controlling the forelimb in the cat. 16. Visually guided switching of target-reaching. Exp Brain Res 80:1–11
Arbib MA (1981) Perceptual structures and distributed motor control. In: Brooks VB (ed) Motor control. (Handbook of physiology, section 1, The nervous system, vol II. Williams and Wilkins, Baltimore, pp 1449–1480
Arbib MA, Iberall T, Lyons D (1985) Coordinated control programs for movements of the hand. Exp Brain Res [Suppl] 10:111–129
Atkeson CG, Hollerbach JM (1985) Kinematic features of unrestrained vertical arm movements. J Neurosci 5:(9) 2318–2330
Bernstein N (1967) The coordination and regulation of movements. Pergamon, Oxford
Bootsma RJ, Marteniuk RG, MaKenzie CL, Zaal FT (1994) The speed-accuracy trade-off in manual prehension: effects of movement amplitude, object size and object width on kinematic characteristics. Exp Brain Res 98:535–541
Brinkman J, Kuypers H (1972) Splitbrain monkeys: cerebral control of ipsilateral and controlateral arm, hand, and finger movements. Science 176:536–539
Castiello U, Bennett KMB, Paulignan Y (1992) Does the type of prehension influence the kinematics of reaching? Behav Brain Res 50:7–15
Chieffi S, Gentilucci M (1993) Coordination between the transport and the grasp components during prehension movements. Exp Brain Res 94:471–477
Chieffi S, Gentilluci M, Allport A, Sasso E, Rizzolatti G (1993) Study of selective reaching and grasping in a patient with unilateral parietal lesion. Brain 116:1119–1137
Colebatch JG, Gandevia SC (1989) The distribution of muscular weakness in upper motor neuron lesions affecting the arm. Brain 112:749–763
Cruse H (1986) Constraints for joint angle control of the human arm. Biol Cybern 54:125–132
Cruse H, Wishmeyer E, Brüwer M, Brockfeld P, Dress A (1990) On the cost functions for the control of the human arm movement. Biol Cybern 62:519–528
Desmurget M, Paulignan Y, Urquizar C, Prablanc C (1994) Aspect of multi-joint flexibility in a power grip task. 17th Annual Meeting of European Neurosciences Association, Vienna
Desmurget M, Prablanc C, Rossetti Y, Arzi M, Paulignan Y, Urquizar C (1995) Postural and synergic control for three dimensionnal movements of reaching and grasping. J Neurophysiol 74:905–910
Fikes TG, Klatzky R, Lederman SJ (1994) Effects of object texture on precontact movement time in human prehension. J Mot Behav 26:325–332
Fitts P (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47:381–391
Flanders M, Tillery SIH, Soechting JF (1992) Early stages in a sensorimotor transformation. Behav Brain Sci 15:309–362
Flash T, Hogan N (1985) The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci 5:1688–1703
Gallese V, Murata A, Kaseda M, Niki N, Sakata H (1994) Deficit of hand preshaping after muscimol injection in monkey parietal cortex. Neuroreport 5:1525–1529
Gentilucci M, Rizzolatti G (1990) Cortical control of arm and hand movements. In: Goodale M (ed) Vision and action: the control of grasping. Norwood, NJ, pp 147–162
Gentilucci M, Fogassi L, Lupino G, Matelli M, Camarda R, Rizzolatti G (1988) Functional organisation of the inferior area 6 in the macaque monkey. I. Somatotopy and control of proximal movements. Exp Brain Res 71:475–490
Gentilucci M, Castiello U, Corradini ML, Scarpa M, Umilta C, Rizzolatti G (1991) Influence of different types of grasping on the transport component of prehension movements. Neuropsychologia 29:361–378
Gentilucci M, Chieffi S, Scarpa M, Castiello U (1992) Temporal coupling between transport and grasp components during prehension movements: effects of visual perturbation. Behav Brain Res 47:71–82
Gordon J, Ghilardi MF, Ghez C (1994) Accuracy of planar reaching movements. 1. Independence of direction and extent variability. Exp Brain Res 99: 97–111
Haggard P, Wing AM (1991) Remote responses to perturbation in human prehension. Neurosci Letters 122:103–108
Haggard P, Wing A (1995) Coordinated responses folowing mechanical perturbation of the arm during prehension. Exp Brain Res 102:483–494
Hoff B, Arbib M (1993) Models of trajectory formation and temporal interaction of reach and grasp. J Mot Behav 25:(3) 175–192
Hogan N, Mussa-Ivaldi F (1992) Muscle behavior may solve motor coordination problems. In: Berthoz A, Graf W, Vidal P (eds) Eye-hand sensori-motor system. Oxford University Press, Oxford, pp 153–157
Hollerbach JM (1988) Fundamentals of motor behavior. In: Osherson D (ed) Invitation to cognitive science. MIT Press, Cambridge, MA, Chap. 16
Hollerbach JM, Atkeson CG (1986) Characterization of joint-Interpolated arm movements. In: Heuer H, Fromm C (eds) Generation and modulation of action patterns. (Exp Brain Res Series 15). Springer, Berlin Heidelberg New York, pp 41–54
Hollerbach JM, Flash T (1982) Dynamic interactions between limb segments during planar movements. Biol Cybern 44:67–77
Hore J, Watts S, Vilis T (1992) Constraints on arm position when pointing in three dimensions: Donders' law and the Fick gimbal strategy. J Neurophysiol 68:374–383
Hore J, Watts S, Tweed D (1994) Arm position constraints when throwing in three dimensions. J Neurophysiol 72:1171–1180
Jakobson LS, Goodale MA (1991) Factors affecting higher-order movement planning: a kinematic analysis of human prehension. Exp Brain Res 86:199–208
Jeannerod M (1981) Intersegmental coordination during reaching at natural visual objects. In: Long J, Baddeley A (eds) Attention and performance. Erlbaum, Hillsdale, pp 153–168
Jeannerod M (1984) The timing of natural prehension. J Mot Behav 16:235–254
Jeannerod M (1986) Mechanisms of visuomotor coordination: a study in normal and brain-damaged subjects. Neuropsychologia 24:41–78
Jeannerod M (1988) The neural and behavioural organization of goal-directed movements. Clarendon, Oxford
Jeannerod M (1992) Coordination mechanisms in prehension movements. In: Stelmach GE, Requin J (ed) Tutorials in motor behavior II. Elsevier Science, Amsterdam, pp 265–285
Jeannerod M (1994) The hand and the object: the role of posterior parietal cortex in forming motor representations. Can J Physiol Pharmacol 72:535–541
Jeannerod M, Biguer B (1982) Visuomotor mechanisms in reaching within extrapersonnal space. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT Press, Cambridge, MA, pp 387–409
Jeannerod M, Decety J, Michel F (1994) Impairment of grasping movements following a bilateral posterior parietal lesion. Neuropsychologia 22:369–380
Kawashima R, Itoh H, Ono S, Satoh K, Furumoto S, Gotoh R, Koyama M, Yoshioka S, Takahashi T, Yanagisawa T, Fukuda H (1995) Activity in the human primary cortex related to arm and finger movements. Neuroreport 6:238–240
Lacquaniti F, Maioli C (1994a) Independent control of limb position and contact forces in cat posture. J Neurophysiol 72:1476–1495
Lacquaniti F, Maioli C (1994b) Coordinate transformations in the control of cat posture. J Neurophysiol 72:1496–1515
Lacquaniti F, Soechting JF (1982) Coordination of arm and wrist motion during a reaching task. J Neurosci 2:399–08
MacKay WA (1992) Properties of reach related neuronal activity in cortical area 7a. J Neurophysiol 67:1335–1345
Marteniuk RG, MacKenzie CL (1990) Invariance and variability in human prehension: implications for theory development. In: Goodale M (ed) Vision and action: the control of grasping. Ablex, Norwood, NJ, pp 49–64
Miller LE, Theeuwen M, Gielen CCAM (1992) The control of arm pointing movements in three dimensions. Exp Brain Res 90:415–26
Morasso P (1981) Spatial control of arm movements. Exp Brain Res 42:223–227
Napier (1956) The prehensible movements of the human hand. J Bone Jt Surg 38B:902–913
Palastanga N., Field D, Soames R (1994) Anatomy and human movement: structure and functions. Butterworth-Heinemann, Oxford
Paulignan Y, Jeannerod M (in press) Prehension movements: the visuomotor channels hypothesis revisited. In: Haggard P, Flanagan R, Wing A (eds) Hand and brain: neurophysiology and psychology of hand movement. Academic, Orlando
Paulignan Y, MacKenzie C, Marteniuk R, Jeannerod M (1991a) Selective perturbation of visual input during prehension movements. 1. The effects of changing object position. Exp Brain Res 83:502–512
Paulignan Y, Jeannerod M, MacKenzie C, Marteniuk R (1991b) Selective perturbation of visual input during prehension movements. 2. The effects of changing object size. Exp Brain Res 87:407–420
Plaget J (1973) Biologie et connaissance. Gallimard, Paris
Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67:455–469
Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functionnal organisation of the inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res 71:490–507
Rosenbaum DA, Engelbrecht SE, Bushe MM, Loukopoulos LD (1993) Knowledge model for selecting and producing reaching movements. J Mot Behav 25:217–227
Rossetti Y, Meckler C, Prablanc C (1994) Is there an optimal arm posture? Deterioration of finger localization precision and comfort sensation in extreme arm-joint postures. Exp Brain Res 99:131–136
Soechting JF (1984) Effect of target size on spatial and temporal characteristics of a pointing movement in man. Exp Brain Res 54:121–132
Soechting JF, Flanders M (1993) Parallel, interdependent channels for location and orientation in sensorimotor transformations for reaching and grasping. J Neurophysiol 70:1137–1150
Soechting JF, Lacquaniti F (1983) Modification of trajectory of a pointing movement in response to a change in target location. J Neurophysiol 49:548–564
Stelmach GE, Castiello U, Jeannerod M (1994) Orienting the finger opposition space during prehension movements. J Mot Behav 26:178–186
Straumnn D, Haslwanter T, Hepp-Reymond M-C, Hepp K (1991) Listing's law for eye, head and arm movements and their synergistic control. Exp Brain Res 86:209–215
Taira M, Mine S, Georgopoulos AP, Murata A, Sakata H (1990) Parietal cortex neurons of the monkey related to the visual guidance of hand movements. Exp Brain Res 83:29–36
Vercher JL, Magenes G, Prablanc C, Gauthier GM (1994) Eye-head-hand coordination in pointing at visual targets: spatial and temporal analysis. Exp Brain Res 99:507–523
Wallace SA, Weeks DL (1988) Temporal constraints in the control of prehensile movement. J Mot Behav 20:81–105
Wing AM, Fraser C (1983) The contribution of the thumb to reaching movements. Q J Exp Psychol 35A:297–309
Zaal FTJM, Bootsma RJ (1993) Accuracy demands in natural prehension. Hum Mov Sci 12:339–345
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Desmurget, M., Prablanc, C., Arzi, M. et al. Integrated control of hand transport and orientation during prehension movements. Exp Brain Res 110, 265–278 (1996). https://doi.org/10.1007/BF00228557
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DOI: https://doi.org/10.1007/BF00228557