Effects of accuracy constraints on reach-to-grasp movements in cerebellar patients

Reach-to-grasp movements of patients with pathology restricted to the cerebellum were compared with those of normal controls. Two types of paradigms with different accuracy constraints were used to examine whether cerebellar impairment disrupts the stereotypic relationship between arm transport and grip aperture and whether the variability of this relationship is altered when greater accuracy is required. The movements were made to either a vertical dowel or to a cross bar of a small cross. All subjects were asked to reach for either target at a fast but comfortable speed, grasp the object between the index finger and thumb, and lift it a short distance off the table. In terms of the relationship between arm transport and grip aperture, the control subjects showed a high consistency in grip aperture and wrist velocity profiles from trial to trial for movements to both the dowel and the cross. The relationship between the maximum velocity of the wrist and the time at which grip aperture was maximal during the reach was highly consistent throughout the experiment. In contrast, the time of maximum grip aperture and maximum wrist velocity of the cerebellar patients was quite variable from trial to trial, and the relationship of these measurements also varied considerably. These abnormalities were present regardless of the accuracy requirement. In addition, the cerebellar patients required a significantly longer time to grasp and lift the objects than the control subjects. Furthermore, the patients exhibited a greater grip aperture during reach than the controls. These data indicate that the cerebellum contributes substantially to the coordination of movements required to perform reach-to-grasp movements. Specifically, the cerebellum is critical for executing this behavior with a consistent, well-timed relationship between the transport and grasp components. This contribution is apparent even when accuracy demands are minimal.

[1]  A R Gibson,et al.  The importance of hand use to discharge of interpositus neurones of the monkey. , 1994, The Journal of physiology.

[2]  W. T. Thach.  A Role for the Cerebellum in Learning Movement Coordination , 1998, Neurobiology of Learning and Memory.

[3]  M. Hallett,et al.  Timing of onset of afferent responses and of use of kinesthetic information for control of movement in normal and cerebellar-impaired subjects , 2006, Experimental Brain Research.

[4]  J. Dichgans,et al.  Dyscoordination of pinch and lift forces during grasp in patients with cerebellar lesions , 2004, Experimental Brain Research.

[5]  M. Gentilucci,et al.  The control of an action in Parkinson’s disease , 1999, Experimental Brain Research.

[6]  U. Castiello,et al.  The reach-to-grasp movement in Parkinson’s disease: response to a simultaneous perturbation of object position and object size , 1999, Experimental Brain Research.

[7]  J. Houk,et al.  Output organization of intermediate cerebellum of the monkey. , 1993, Journal of neurophysiology.

[8]  H. Diener,et al.  Clinical Evidence for Functional Compartmentalization of the Cerebellum , 1984 .

[9]  M. Hallett,et al.  Disturbances of kinaesthesia in patients with cerebellar disorders. , 1994, Brain : a journal of neurology.

[10]  M. Hallett,et al.  Physiological analysis of simple rapid movements in patients with cerebellar deficits. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[11]  V. Brooks,et al.  Effects of dentate cooling on rapid alternating arm movements. , 1974, Journal of neurophysiology.

[12]  C. MacKenzie,et al.  Integration of visual information and motor output in reaching and grasping: The contributions of peripheral and central vision , 1990, Neuropsychologia.

[13]  W. T. Thach,et al.  Cerebellar nuclei: rapid alternating movement, motor somatotopy, and a mechanism for the control of muscle synergy. , 1993, Revue neurologique.

[14]  Richard lvry,et al.  Cerebellar timing systems. , 1997 .

[15]  Okihide Hikosaka,et al.  Presaccadic omnidirectional burst activity in the basal interstitial nucleus in the monkey cerebellum , 1998, Experimental Brain Research.

[16]  G. Stelmach,et al.  Grip reorganization during wrist transport: the influence of an Altered aperture , 1996, Experimental Brain Research.

[17]  G. Holmes.  THE CEREBELLUM OF MAN , 1939 .

[18]  R. Lee,et al.  Spatio-temporal and kinematic analysis of pointing movements performed by cerebellar patients with limb ataxia , 1998, Experimental Brain Research.

[19]  M. Jeannerod,et al.  Orienting the finger opposition space during prehension movements. , 1994, Journal of motor behavior.

[20]  W. T. Thach,et al.  Cerebellar ataxia: abnormal control of interaction torques across multiple joints. , 1996, Journal of neurophysiology.

[21]  O. Hikosaka,et al.  Role of monkey cerebellar nuclei in skill for sequential movement. , 1998, Journal of neurophysiology.

[22]  C Dohle,et al.  Human anterior intraparietal area subserves prehension , 1998, Neurology.

[23]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[24]  S. Keele,et al.  Dissociation of the lateral and medial cerebellum in movement timing and movement execution , 2004, Experimental Brain Research.

[25]  W. T. Thach,et al.  Cerebellar outflow lesions: A comparison of movement deficits resulting from lesions at the levels of the cerebellum and thalamus , 1995, Annals of neurology.

[26]  A. Wing,et al.  Impaired anticipatory finger grip-force adjustments in a case of cerebellar degeneration , 1999, Experimental Brain Research.

[27]  J. A. Scott Kelso,et al.  Temporal constraints in reaching and grasping behavior , 1990 .

[28]  M. Wiesendanger,et al.  Role of the Cerebellum in Tuning Anticipatory and Reactive Grip Force Responses , 1999, Journal of Cognitive Neuroscience.

[29]  M. Jeannerod,et al.  Impairment of grasping movements following a bilateral posterior parietal lesion , 1994, Neuropsychologia.

[30]  G E Stelmach,et al.  Impaired capacity of cerebellar patients to perceive and learn two-dimensional shapes based on kinesthetic cues. , 1997, Learning & memory.

[31]  R. Ivry,et al.  The role of cerebellar structures in the execution of serial movements. , 1989, Brain : a journal of neurology.

[32]  W T Thach,et al.  The cerebellum and the adaptive coordination of movement. , 1992, Annual review of neuroscience.

[33]  G. Stelmach,et al.  Ataxia reflected in the simulated movements of patients with cerebellar lesions , 1998, Experimental Brain Research.

[34]  Umberto Castiello,et al.  Parkinson's disease: reorganization of the reach to grasp movement in response to perturbation of the distal motor patterning , 1994, Neuropsychologia.

[35]  M. Jeannerod.  Intersegmental coordination during reaching at natural visual objects , 1981 .

[36]  M Hallett,et al.  Kinematics of Initiating a Two-Joint Arm Movement in Patients with Cerebellar Ataxia , 1996, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[37]  J. Bloedel,et al.  On the cerebellum, cutaneomuscular reflexes, movement control and the elusive engrams of memory , 1995, Behavioural Brain Research.

[38]  Christine L. MacKenzie,et al.  Functional relationships between grasp and transport components in a prehension task , 1990 .

[39]  A. Wing,et al.  Grasp size and accuracy of approach in reaching. , 1986, Journal of motor behavior.

[40]  Coordination between the transport and the grasp during prehension movements , 1993 .

[41]  J. Konczak,et al.  Multijoint arm movements in cerebellar ataxia: Abnormal control of movement dynamics , 1998, Experimental Brain Research.

[42]  A R Gibson,et al.  Construction of a reach-to-grasp. , 2007, Novartis Foundation symposium.

[43]  J. R. Bloedel,et al.  Adaptive changes in responses to repeated locomotor perturbations in cerebellar patients , 1998, Experimental Brain Research.

[44]  J. Hore,et al.  Movement and electromyographic disorders associated with cerebellar dysmetria. , 1986, Journal of neurophysiology.

[45]  E. Trouche,et al.  Initiation of a goal-directed movement in the monkey , 1980, Experimental Brain Research.

[46]  H. Diener,et al.  Control of isometric finger force in patients with cerebellar disease. , 1988, Brain : a journal of neurology.

[47]  A. Wing,et al.  Coordination of aimed movements in a case of unilateral cerebellar damage , 1994, Neuropsychologia.

[48]  M Jeannerod,et al.  Grasping an object: one movement, several components. , 1998, Novartis Foundation symposium.

[49]  V Bracha,et al.  Patients with cerebellar lesions cannot acquire but are able to retain conditioned eyeblink reflexes. , 1997, Brain : a journal of neurology.

[50]  A R Gibson,et al.  Activity of interpositus neurons during a visually guided reach. , 1996, Canadian journal of physiology and pharmacology.

[51]  M. Jeannerod,et al.  Selective perturbation of visual input during prehension movements , 2004, Experimental Brain Research.

[52]  D Timmann,et al.  Failure of cerebellar patients to time finger opening precisely causes ball high-low inaccuracy in overarm throws. , 1999, Journal of neurophysiology.

[53]  R. G. Lee,et al.  Multi-Joint Reaching Movements and Eye-Hand Tracking in Cerebellar Incoordination: Investigation of a Patient with Complete Loss of Purkinje Cells , 1991, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[54]  R. Ivry.  Cerebellar timing systems. , 1997, International review of neurobiology.

[55]  M. Jeannerod,et al.  Influence of object position and size on human prehension movements , 1997, Experimental Brain Research.

[56]  E. Trouche,et al.  Participation of the cerebellar dentate nucleus in the control of a goal-directed movement in monkeys , 1982, Experimental Brain Research.

[57]  J. Hore,et al.  Cerebellar dysmetria at the elbow, wrist, and fingers. , 1991, Journal of neurophysiology.

[58]  W. T. Thach,et al.  Preserved Simple and Impaired Compound Movement After Infarction in the Territory of the Superior Cerebellar Artery , 1993, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[59]  J. R. Bloedel,et al.  Grasping component alterations and limb transport , 1996, Experimental Brain Research.

[60]  M. Jeannerod,et al.  Selective perturbation of visual input during prehension movements , 1991, Experimental Brain Research.

[61]  J. Konczak,et al.  Coordination of multi-joint arm movements in cerebellar ataxia: Analysis of hand and angular kinematics , 1998, Experimental Brain Research.

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

[63]  O Hikosaka,et al.  Neural Representation of a Rhythm Depends on Its Interval Ratio , 1999, The Journal of Neuroscience.

[64]  G. Stelmach,et al.  Visuomotor learning in cerebellar patients , 1996, Behavioural Brain Research.

[65]  S Gilman,et al.  Kinematic effects of deafferentation and cerebellar ablation. , 1976, Brain : a journal of neurology.

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

[67]  Y Shimansky,et al.  Effects of inactivating individual cerebellar nuclei on the performance and retention of an operantly conditioned forelimb movement. , 1997, Journal of neurophysiology.

[68]  Norio Fujimaki,et al.  Separate cerebellar areas for motor control , 1998, Neuroreport.

[69]  J. F. Soechting,et al.  Gradual molding of the hand to object contours. , 1998, Journal of neurophysiology.

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

[71]  M Jeannerod,et al.  Visual pathways for object-oriented action and object recognition: functional anatomy with PET. , 1997, Cerebral cortex.