Differential effects of deep cerebellar nuclei inactivation on reaching and adaptive control.

This study examined the effects of selective inactivation of the cerebellar nuclei in the cat on the control of multijoint trajectories and trajectory adaptation to avoid obstacles. Animals were restrained in a hammock and trained to perform a prehension task in which they reached to grasp a small cube of meat from a narrow food well. To examine trajectory adaptation, reaching was obstructed by placing a horizontal bar in the limb's path. Inactivation was produced by microinjection of the GABA agonist muscimol (0.25-1.0 microg in 1 microL saline). Fastigial nucleus inactivation produced a severe impairment in balance and in head and trunk control but no effect on reaching and grasping. Dentate inactivation slowed movements significantly and produced a significant increase in tip path curvature but did not impair reaching and grasping. Selective inactivation of the anterior and posterior interpositus nuclei did not impair grasping but severely decreased the accuracy of reaching movements and produced different biases in wrist and paw paths. Anterior interpositus inactivation produced movement slowing (wrist speed) and under-reaching to the food well. Wrist and tip paths showed anterior biases and became more curved. Also animals could no longer make anticipatory adjustments in limb kinematics to avoid obstructions but sensory-evoked corrective responses were preserved. Posterior interpositus inactivation produced a significant increase in wrist speed and overreaching. Wrist and tip paths showed a posterior bias and became more curved, although in a different way than during anterior interpositus inactivation. Posterior interpositus inactivation did not impair trajectory adaptation to reach over the obstacle. During inactivation of either interpositus nucleus, all measures of kinematic temporal and spatial variability increased with somewhat greater effects being produced by anterior interpositus inactivation. We discuss our results in relation to the hypothesis that anterior and posterior interpositus have different roles in trajectory control, related possibly to feed-forward use of cutaneous and proprioceptive inputs, respectively. The loss of adaptive reprogramming during anterior interpositus inactivation further suggests a role in motor learning. Comparison with results from our earlier motor cortical study shows that the distinctive impairments produced by inactivation of these two nuclei are similar to those produced by selective inactivation of different zones in the forelimb area of rostral motor cortex. Our findings are consistent with the hypothesis that there are separate functional output channels from the anterior and posterior interpositus nuclei to rostral motor cortex for distinct aspects of trajectory control and, from anterior interpositus alone, for trajectory adaptation.

[1]  W. Chambers,et al.  Functional localization in the cerebellum. I. Organization in longitudinal cortico‐nuclear zones and their contribution to the control of posture, both extrapyramidal and pyramidal , 1955, The Journal of comparative neurology.

[2]  V. Brooks,et al.  Effects of cooling interposed nuclei on tracking-task performance in monkeys. , 1973, Journal of neurophysiology.

[3]  G. Berntson,et al.  An atlas of the deep cerebellar nuclei and subtentorial brainstem of the cat with compensation for skull-size , 1978, Brain Research Bulletin.

[4]  H. Forssberg Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion. , 1979, Journal of neurophysiology.

[5]  E. Sybirska,et al.  Effects of pyramidal lesions on forelimb movements in the cat. , 1980, Acta neurobiologiae experimentalis.

[6]  K. Nakano,et al.  Distribution of cerebellothalamic neurons projecting to the ventral nuclei of the thalamus: An HRP study in the cat , 1980, The Journal of comparative neurology.

[7]  T. Vilis,et al.  Central neural mechanisms contributing to cerebellar tremor produced by limb perturbations. , 1980, Journal of neurophysiology.

[8]  B Alstermark,et al.  Integration in descending motor pathways controlling the forelimb in the cat. 9. Differential behavioural defects after spinal cord lesions interrupting defined pathways from higher centres to motoneurones. , 1981, Experimental brain research.

[9]  D. Tolhurst,et al.  The thalamus and basal telencephalon of the cat by A.L. Berman and E.G. Jones, University of Wisconsin Press, 1982. £162.50 (xvi + 156 pages) ISBN 299 08440 X , 1982, Trends in Neurosciences.

[10]  E. Jones,et al.  The thalamus and basal telencephalon of the cat: A cytoarchitectonic atlas with stereotaxic Coordinates , 1982 .

[11]  W. T. Thach,et al.  Anatomical evidence for segregated focal groupings of efferent cells and their terminal ramifications in the cerebellothalamic pathway of the monkey , 1983, Brain Research Reviews.

[12]  J. Houk,et al.  Somatosensory properties of the inferior olive of the cat , 1983, The Journal of comparative neurology.

[13]  Y. Shinoda,et al.  Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat. I. Projection of individual cerebellar nuclei to single pyramidal tract neurons in areas 4 and 6 , 1985, Neuroscience Research.

[14]  J. F. Stein,et al.  Role of the cerebellum in the visual guidance of movement , 1986, Nature.

[15]  M. Hoy,et al.  The role of intersegmental dynamics during rapid limb oscillations. , 1986, Journal of biomechanics.

[16]  Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat : cerebellar input to corticofugal neurons destined for different subcortical nuclei in areas 4 and 6 , 1986 .

[17]  J. Houk,et al.  Somatotopic alignment between climbing fiber input and nuclear output of the cat intermediate cerebellum , 1987, The Journal of comparative neurology.

[18]  John H. Martin Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat , 1991, Neuroscience Letters.

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

[20]  J. L. Taylor,et al.  Cerebellar ataxia and muscle spindle sensitivity. , 1993, Journal of neurophysiology.

[21]  R L Sainburg,et al.  Control of limb dynamics in normal subjects and patients without proprioception. , 1995, Journal of neurophysiology.

[22]  Claude Ghez,et al.  Kinematic and Dynamic Factors in the Coordination of Prehension Movements , 1996 .

[23]  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.

[24]  J F Baker,et al.  Organization of reaching and grasping movements in the primate cerebellar nuclei as revealed by focal muscimol inactivations. , 1998, Journal of neurophysiology.

[25]  P. Strick,et al.  Cerebellar output: motor and cognitive channels , 1998, Trends in Cognitive Sciences.

[26]  D. Armstrong,et al.  Zonal organization of cortico-nuclear and nucleo-cortical projections of the paramedian lobule of the cat cerebellum. 2. The C2 zone , 1998, Experimental Brain Research.

[27]  H. Jörntell,et al.  Topographical organization of projections to cat motor cortex from nucleus interpositus anterior and forelimb skin , 1999, The Journal of physiology.

[28]  C. Ghez,et al.  Pharmacological inactivation in the analysis of the central control of movement , 1999, Journal of Neuroscience Methods.

[29]  P. Strick,et al.  The Organization of Cerebellar and Basal Ganglia Outputs to Primary Motor Cortex as Revealed by Retrograde Transneuronal Transport of Herpes Simplex Virus Type 1 , 1999, The Journal of Neuroscience.