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Initiation of a goal-directed movement in the monkey

Role of the cerebellar dentate nucleus

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Summary

The participation of the dentate nucleus (DN) in the initiation of a voluntary movement was investigated in five baboons (Papio papio). In these experiments, we have analyzed the effects of excluding the DN on the latency (reaction time, RT) of a learned goal-directed movement.

Two techniques were used for excluding the DN. In three animals, the structure was cooled with a probe, stereotaxically implanted on the side ipsilateral to the active hand. In two others, a partial electrolytic destruction of the DN ipsilateral to the operant hand was undertaken. In one further animal, both DNs were destroyed electrolytically.

A comparison was made of the effect of DN inactivation on the latency of stereotyped goal-directed movements of constant amplitude and direction, and of goal-directed movements whose amplitude and/or direction were varied in random fashion.

The exclusion of DN brought about a prolongation of RTs in all animals. This prolongation was not accentuated by variation of different characteristics (amplitude and/or direction) of the impending goal-directed movement.

A recovery of the RTs to their prelesion values was observed after irreversible unilateral DN lesion, but not so easily after bilateral destruction.

These results show that in the monkey DN is concerned with the initiation of a goal-directed movement, but is not critically implicated in the encoding of direction and amplitude parameters. These findings are discussed in view of the role that is usually attributed to the neocerebellum in programming voluntary movements.

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References

  • Allen GI, Gilbert PFC, Yin TCT (1978) Convergence of cerebral inputs onto dentate neurons in monkey. Exp Brain Res 32: 151–170

    Google Scholar 

  • Allen GI, Tsukahara N (1974) Cerebro-cerebellar communication systems. Physiol Rev 54: 957–1006

    CAS  PubMed  Google Scholar 

  • Angaut P (1979) The cerebello-thalamic projections in the cat. In: Massion J, Sasaki K (eds) Cerebro-cerebellar interactions. Developments in neuroscience, vol 6. Elsevier, Amsterdam, pp 19–43

    Google Scholar 

  • Bantli H, Bloedel JR (1976) Characteristics of the output from the dentate nucleus to spinal neurons via pathways which do not involve the primary sensorimotor cortex. Exp Brain Res 25: 199–220

    Google Scholar 

  • Beaubaton D, Requin J (1972) The time course of preparatory processes in split-brain monkeys performing a variable foreperiod reaction time task. Physiol Behav 10: 725–730

    Google Scholar 

  • Beaubaton D, Trouche E, Amato G (1980) (in press) Dentate and pallidal control of a goal directed movement in monkeys. In: Stelmach GE, Requin J (eds) Tutorials in motor behavior. Elsevier, Amsterdam

    Google Scholar 

  • Beaubaton D, Trouche E, Amato G, Grangetto A (1978) Dentate cooling in monkeys performing a visuo-motor pointing task. Neurosci Letters 8: 225–229

    Google Scholar 

  • Benita M (1972) Nouveau dispositif pour le refroidissement localisé des structures nerveuses. Electroencephal Clin Neurophysiol 32: 90–94

    Google Scholar 

  • Benita M, Condé H, Dormont JF, Schmied A (1979) Effects of ventrolateral thalamic nucleus cooling on initiation of forelimb ballistic flexion movements by conditioned cats. Exp Brain Res 34: 435–452

    Google Scholar 

  • Brooks VB (1979a) Motor programs revisited. In: Talbott RE, Humphrey DR (eds) Posture and movement. Perspectives for integrating sensory and motor research on the mammalian nervous system. Raven Press, New York, pp 13–49

    Google Scholar 

  • Brooks VB (1979b) Control of intended limb movement by the lateral and intermediate cerebellum. In: Asanuma H, Wilson VJ (eds) Integration in the nervous system. Igaku-Shoin, Tokyo New York, pp 321–356

    Google Scholar 

  • Brooks VB, Kozlovskaya IB, Atkin A, Horvath FE, Uno M (1973) Effects of cooling dentate nucleus on tracking task performance in monkeys. J Neurophysiol 36: 974–995

    Google Scholar 

  • Carpenter MB, Strominger NL (1964) Cerebello-oculomotor fibers in the rhesus monkey. J Comp Neurol 123: 211–230

    Google Scholar 

  • Carrea RME, Mettler FA (1947) Physiologic consequences following extensive removal of the cerebellar cortex and deep cerebellar nuclei and effect of secondary cerebral ablations in the primate. J Comp Neurol 87: 169–288

    Google Scholar 

  • Chan-Palay V (1977) Cerebellar dentate nucleus. Springer, Berlin Heidelberg New York, pp 548

    Google Scholar 

  • Dondey M, Albe-Fessard D, Le Beau J (1962) Premières applications neurophysiologiques d'une méthode permettant le blocage électif et reversible de structures centrales par réfrigération localisée. Electroencephal Clin Neurophysiol 14: 758–763

    Google Scholar 

  • Evarts EV (1968) Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol 31: 14–27

    Google Scholar 

  • Evarts EV, Thach WT (1969) Motor mechanisms of the CNS. Cerebro-cerebellar interrelations. Ann Rev Physiol 31: 451–498

    Google Scholar 

  • Fulton JF, Dow RS (1937) The cerebellum. A summary of functional localization. Yale J Biol Med 10: 89–119

    Google Scholar 

  • Gardner EP, Fuchs AF (1975) Single-unit responses to natural vestibular stimuli and eye movement in deep cerebellar nuclei of the alert rhesus monkey. J Neurophysiol 38: 627–649

    Google Scholar 

  • Goldberger ME (1974) Recovery of movement after CNS lesions in monkeys. In: Stein DJ, Rosen JJ, Butters N (eds) Plasticity and recovery of function in the central nervous system. Academic Press, New York, pp 265–337

    Google Scholar 

  • Goldberger ME, Growdon JH (1973) Pattern of recovery following cerebellar deep nuclear lesions in monkeys. Exp Neurol 39: 307–322

    Google Scholar 

  • Grimm RJ, Rushmer DS (1974) The activity of dentate neurons during an arm movement sequence. Brain Res 71: 309–326

    Google Scholar 

  • Growdon JH, Chambers WW, Liu CN (1967) An experimental study of cerebellar dyskinesia in the rhesus monkey. Brain 90: 603–632

    Google Scholar 

  • Hallett M, Shahani BT, Young RR (1975) EMG analysis of patients with cerebellar deficits. J Neurol Neurosurg Psychiatry 38: 1163–1169

    Google Scholar 

  • Heidary H, Tomasch J (1969) Neuron numbers and perikaryon areas in the human cerebellar nuclei. Acta Anat (Basel) 74: 290–296

    Google Scholar 

  • Holmes G (1917) The symptoms of acute cerebellar injuries due to gunshot injuries. Brain 40: 461–535

    Google Scholar 

  • Holmes G (1939) The cerebellum of man. Brain 62: 1–30

    Google Scholar 

  • Keele SW (1968) Movement control in skilled motor performance. Psychol Bull 70: 387–403

    Google Scholar 

  • Kornhuber HH (1971) Motor function of the cerebellum and basal ganglia: the cerebello-cortical saccadic (ballistic) clock, the cerebello-nuclear hold regulator, and the basal ganglia ramp (voluntary speed smooth movement) generator. Kybernetik 8: 157–162

    Google Scholar 

  • Lamarre Y, Spidalieri G, Busby L (1979) Effects of dentate lesion on discharge pattern of motor cortex neurons. Soc Neurosci Abstr 5: 1257

    Google Scholar 

  • Massarino R, Trouche E, Beaubaton D (1979a) Self-contained dual chronic cryoprobe for deep neural structures. Physiol Behav 22: 1021–1023

    Google Scholar 

  • Massarino R, Poveda G, Beaubaton D, Trouche E (1979b) Boîte de manipulation pour la mesure de performances motrices mettant en jeu la musculature distale du membre antérieur chez les primates. Physiol Behav 23: 27–30

    Google Scholar 

  • Massion J (1973) Intervention des voies cérébello-corticales et cortico-cérébelleuses dans l'organisation et la régulation du mouvement. J Physiol (Paris) 67: 117A-170A

    Google Scholar 

  • Massion J, Sasaki K (1979) Cerebro-cerebellar interaction. Solved and unsolved problems. In: Massion J, Sasaki K (eds) Cerebro-cerebellar interactions. Developments in neurosciences, vol 6. Elsevier, Amsterdam, pp 261–287

    Google Scholar 

  • Meyer-Lohmann J, Conrad B, Matsunami K, Brooks VB (1975) Effects of dentate cooling on precentral unit activity following torque pulse injections into elbow movements. Brain Res 94: 237–251

    Google Scholar 

  • Meyer-Lohmann J, Höre J, Brooks VB (1977) Cerebellar participation in generation of prompt arm movements. J Neurophysiol 40: 1038–1050

    Google Scholar 

  • Miller AD, Brooks VB (1977) Effects of cooling ventral lateral thalamus (VL) and sensori-motor cortex on long-loop reflexes in monkey. Soc Neurosci Abstr 3: 274

    Google Scholar 

  • Nashold BS, Slaughter DG (1969) Effects of stimulating or destroying the deep cerebellar region in man. J Neurosurg 31: 172–186

    Google Scholar 

  • Paillard J (1980) (in press) The contribution of peripheral and central vision to visually guided reaching. In: Ingle DJ, Goodale MS (eds) Advances in the analysis of visual behavior. MIT Press, Cambridge, MA

    Google Scholar 

  • Paillard J, Beaubaton D (1978) De la coordination visuo-motrice à l'organisation de la saisie manuelle. In: Hécaen H, Jeannerod M (eds) Du contrôle moteur à l'organisation du geste. Masson, Paris, pp 224–260

    Google Scholar 

  • Poirier LJ, Lafleur J, Delfan J, Guiot G, Larochelle L, Boucher R (1974) Physiopathology of the cerebellum in the monkey. II. Motor disturbances associated with partial and complete destruction of cerebellar structures. J Neurol Sci 32: 491–509

    Google Scholar 

  • Polit A, Bizzi E (1979) Characteristics of motor programs underlying arm movements in monkeys. J Neurophysiol 42: 183–194

    Google Scholar 

  • Requin J (1980) (in press) Toward a psychobiology of preparation for action. In: Stelmach GE, Requin J (eds) Tutorials in motor behavior. Elsevier, Amsterdam (in press)

    Google Scholar 

  • Riche D, Courville J, Massion J, Nieoullon A (1971) Stereotaxic anatomy of the cerebellar nuclei in the baboon (Papio papio). J Physiol (Paris) 63: 793–837

    Google Scholar 

  • Robertson LT, Grimm RJ (1975) Responses of primate dentate neurons to different trajectories of the limb. Exp Brain Res 23: 447–462

    Google Scholar 

  • Ron S, Robinson DA (1973) Eye movements evoked by cerebellar stimulation in the alert monkey. J Neurophysiol 36: 1004–1022

    Google Scholar 

  • Rondot P, Bathien N, Toma S (1979) Physiopathology of cerebellar movement. In: Massion J, Sasaki K (eds) Cerebrocerebellar interactions. Developments in neurosciences, vol 6. Elsevier, Amsterdam, pp 203–230

    Google Scholar 

  • Sasaki K (1979) Cerebro-cerebellar interconnections in cats and monkeys. In: Massion J, Sasaki K (eds) Cerebro-cerebellar interactions. Developments in neurosciences, vol 6. Elsevier, Amsterdam, pp 105–124

    Google Scholar 

  • Sasaki K, Jinnai K, Gemba H, Hashimoto S, Mizuno N (1979) Projection of the cerebellar dentate nucleus onto the frontal association cortex in monkeys. Exp Brain Res 37: 193–198

    Google Scholar 

  • Schmied A, Benita M, Condé H, Dormont JF (1979) Activity of ventrolateral thalamic neurons in relation to a simple reaction time task in the cat. Exp Brain Res 36: 285–300

    Google Scholar 

  • Schultz W, Montgomery EB, Marini R (1979) Proximal limb movements in response to microstimulation of primate dentate and interpositus nuclei mediated by brain-stem structures. Brain 102: 127–146

    Google Scholar 

  • Semjen A, Requin J (1976) Movement amplitude, pointing accuracy and choice reaction time. Percept Mot Skills 43: 807–812

    Google Scholar 

  • Stanton GB (1973) Thalamic organization of some dentate and dentate interpositus nucleus projections in Macaca mulatta. Anat Rec 175: 450

    Google Scholar 

  • Strick PL (1976) Activity of ventralateral thalamic neurons during arm movement. J Neurophysiol 39: 1032–1044

    Google Scholar 

  • Strick PL (1979) Control of peripheral input to the dentate nucleus by motor preparation. In: Massion J, Sasaki K (eds) Cerebrocerebellar interactions. Developments in neurosciences, vol 6. Elsevier, Amsterdam, pp 185–201

    Google Scholar 

  • Taub E, Goldberg IA, Taub P (1975) Deafferentation in monkeys pointing at a target without visual feedback. Exp Neurol 46: 178–186

    Google Scholar 

  • Thach WT (1972) Cerebellar output. Properties synthesis and uses. Brain Res 40: 89–97

    Google Scholar 

  • Thach WT (1975) Timing of activity in cerebellar dentate nucleus and cerebral motor cortex during prompt volitional movement. Brain Res 88: 233–241

    Google Scholar 

  • Thach WT (1978) Correlation of neural discharge with pattern and force of muscular activity, joint position and direction of intended next movement in motor cortex and cerebellum. J Neurophysiol 41: 654–676

    Google Scholar 

  • Thach WT, Jones EG (1979) The cerebellar dentatothalamic connection: terminal field, lamellae, rods and somatotopy. Brain Res 169: 168–172

    Google Scholar 

  • Trevarthen C (1972) Specialized lesions. The split brain technique. In: Myers RD (ed) Methods in psychobiology. Academic Press, London, pp 251–294

    Google Scholar 

  • Trouche E, Beaubaton D, Amato G, Grangetto A (1979) Impairements and recovery of the spatial and temporal components of a visuo-motor pointing movement after unilateral destruction of the dentate nucleus in the baboon. Appl Neurophysiol 42: 248–254

    Google Scholar 

  • Uno M, Kozlovskaya IB, Brooks VB (1973) Effects of cooling interposed nuclei on tracking task performance in monkeys. J Neurophysiol 36: 996–1003

    Google Scholar 

  • Verdie J-C (1976) Le noyau dentelé: Données fondamentales. Analyse de 50 cas de dentatomies stéréotaxiques. Thèse de Doctorat d'Etat en Médecine, Toulouse

  • Wiesendanger M, Rüegg DG, Wiesendanger R (1979a) The cortico-pontine system in primates. Anatomical and functional considerations. In: Massion J, Sasaki K (eds) Cerebrocerebellar interactions. Developments in neuroscience, vol 6. Elsevier, Amsterdam, pp 45–65

    Google Scholar 

  • Wiesendanger R, Wiesendanger M, Rüegg DG (1979b) An anatomical investigation of the corticopontine projection in the primate (Macaca Fascicularis and Saimiri sciureus). II. The projection from frontal and parietal association areas. Neuroscience 4: 747–765

    Google Scholar 

  • Zervas NT (1970) Paramedial cerebellar nuclear lesions. Confin Neurol 32: 114–117

    Google Scholar 

  • Zervas NT, Horner FG, Gordy PD (1967) Cerebellar dentatectomy in primates and humans. Trans Am Neurol Assoc 92: 27–29

    Google Scholar 

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  1. Institut de Neurophysiologie et Psychophysiologie, C.N.R.S. - INP 4, 31, chemin Joseph Aiguier, F-13274, Marseille Cedex 2, France

    E. Trouche & D. Beaubaton M.D.

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  1. E. Trouche
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  2. D. Beaubaton M.D.
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This work was in part supported by C.N.R.S. grant (ATP 4187) and INSERM grants (ATP 80.79.112, CRL 79.4.346.6)

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Trouche, E., Beaubaton, D. Initiation of a goal-directed movement in the monkey. Exp Brain Res 40, 311–321 (1980). https://doi.org/10.1007/BF00237796

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