Summary
When the hand of the observer is used as a visual target, oculomotor performance evaluated in terms of tracking accuracy, delay and maximal ocular velocity is higher than when the subject tracks a visual target presented on a screen. The coordination control exerted by the motor system of the arm on the oculomotor system has two sources: the transfer of kinaesthetic information originating in the arm which increases the mutual coupling between the arm and the eyes and information from the arm movement efferent copy which synchronizes the motor activities of both subsystems (Gauthier et al. 1988; Gauthier and Mussa-Ivaldi 1988). We investigated the involvement of the cerebellum in coordination control during a visuo-oculo-manual tracking task. Experiments were conducted on baboons trained to track visual targets with the eyes and/or the hand. The role of the cerebellum was determined by comparing tracking performance defined in terms of delay, accuracy (position or velocity tracking errors) and maximal velocity, before and after lesioning the cerebellar dentate nucleus. Results showed that in the intact animal, ocular tracking was more saccadic when the monkey followed an external target than when it moved the target with its hand. After lesioning, eye-alone tracking of a visual target as well as eye-and-hand-tracking with the hand contralateral to the lesion was little if at all affected. Conversely, ocular tracking of the hand ipsilateral to the lesion side became more saccadic and the correlation between eye and hand movement decreased considerably while the delay between target and eyes increased. In normal animals, the delay between the eyes and the hand was close to zero, and maximal smooth pursuit velocity was around 100 degrees per second with close to unity gain; in eye-alone tracking the delay and maximal smooth pursuit velocity were 200 ms and 50 deg per second, respectively. After lesioning, delay and maximum velocity were respecttively around 210 ms and 40 deg per second, that is close to the values measured in eye-alone tracking. Thus, after dentate lesioning, the oculomotor system was unable to use information from the motor system of the arm to enhance its performance. We conclude that the cerebellum is involved in the “coordination control” between the oculomotor and manual motor systems in visuo-oculo-manual tracking tasks.
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References
Bahill AT, McDonald JD (1983) Smooth pursuit eye movements in response to predictable target motions. Vision Res 23: 1573–1583
Barmack NH (1970) Dynamic visual acuity as an index of eye movement control. Visin Res 10: 1377–1391
Beaubaton D, Hay L (1986) Contribution of visual information to feed-forward and feedback processes in rapid pointing movements. Human Mov Sci 5: 19–34
Beaubaton D, Trouche E, Amato G, Grangetto A (1978) Dentate cooling in monkeys performing a visuo-motor pointing task. Neurosci Lett 8: 225–229
Beaubaton D, Trouche E, Amato G (1980) Dentate and pallidal control of a goal-directed movement in monkeys. In: Stelmach GE, Requin J (eds) Tutorials in motor behavior. North Holland Publishing Co, Amsterdam
Beppu H, Suda M, Tanaka R (1984) Analysis of cerebellar motor disorders by visually guided elbow tracking movement. Brain 107: 787–809
Brooks VB (1979) Control of intended limb movements by the lateral and intermediate cerebellum. In: Asanuma H, Wilson VJ (eds) Integration in the nervous system. Igaku-shoin, Tokyo, New York, pp 321–357
Brooks VB, Kozlovskaya B, Atkin A, Horvath FE, Uno M (1973) Effects of cooling the dentate nucleus on tracking-task performance in monkeys. J Neurophysiol 36: 974–995
Buchtel HA, Iosif G, Marchesi GF, Provini L, Strata P (1972) Analysis of the activity evoked in the cerebellar cortex by stimulation of the visual pathways. Exp Brain Res 15: 278–288
Buchtel HA, Rubia FJ, Strata P (1973) Cerebellar unitary responses to moving visual stimuli. Brain Res 50: 463–466
Buizza A, Schmid R (1986) Velocity characteristics of smooth pursuit eye movements to different patterns of target motion. Exp Brain Res 63: 395–401
Chapman CE, Spidalieri G, Lamarre Y (1986) Activity of dentate neurones during arm movements triggered by visual, auditory, and somesthetic stimuli in the monkey. J Neurophysiol 55: 203–226
Cogan DG, Chu FC, Reingold DB (1982) Ocular signs of cerebellar disease. Arch Ophthalmol 100: 755–760
Conrad B, Brooks VB (1974) Effects of dentate cooling on rapid alternating arm movements. J Neurophysiol 37: 792–804
Conti P, Beaubaton D (1980) Role of structured visual reafference in accuracy of pointing movements. Percept Mot Skills 50: 239–244
Estanol B, Romero R, Corvera J (1979) Effects of cerebellectomy on eye movements in man. Arch Neurol 36: 281–284
Fabre M, Buser P (1981) Effects of lesioning the anterior suprasylvian cortex on visuo-motor guidance performance in the cat. Exp Brain Res 41: 81–88
Fuchs AF (1967) Saccadic and smooth pursuit eye movement in the monkey. J Physiol (London) 191: 609–631
Fuchs AF, Kornhuber HH (1969) Extra-ocular muscle afferents to the cerebellum of the cat. J Physiol (London) 200: 713–722
Gauthier GM, Hofferer JM (1976a) Eye tracking of self-moved target in the absence of vision. Exp Brain Res 26: 121–139
Gauthier GM, Hofferer JM (1976b) Eye movements in response to real and apparent motion of acoustic targets. Percept Mot Skills 42: 963–971
Gauthier GM, Mussa-Ivaldi F (1988) Oculo-manual tracking of visual targets in monkeys: role of the arm afferent information in the control of arm and eye movements. Exp Brain Res 73: 138–154
Gauthier GM, Stark L (1979) Cerebellar stimulation and eye movements in cats. Math Biosci 46: 37–58
Gauthier GM, Hofferer JM, Hoyt WF, Stark L (1979) Visual-motor adaptation. Quantitative demonstration in patients with posterior fossa involvement. Arch Neurol 36: 155–160
Gauthier GM, Vercher J-L, Mussa-Ivaldi F, Marchetti E (1988) Oculo-manual tracking of visual targets: control learning, coordination control and coordination model. Exp Brain Res 73: 127–137
Hay L, Brouchon M (1972) Analyse de la réorganisation des coordinations visuo-motrices chez I'homme. Ann Psychologique 72: 25–38
Holmes G (1917) The symptoms of acute cerebellar injuries due to gunshot injuries. Brain 40: 461–535
Jeannerod M, Prablanc C (1983) Visual control of reaching movements in man. In: Desmedt JE (ed) Motor control mechanisms in health and disease. Advances in Neurology, Vol 39. Raven Press, New York, pp 13–29
Knapp HD, Taub E, Berman AJ (1963) Movements in monkeys with deafferented forelimb. Exp Neurol 7: 305–315
Larmande P, Delplace MP, Autret A (1980) Influence du cervelet sur la statique oculaire et les mouvements de poursuite visuelle. Rev Neurol (Paris) 136: 327–339
Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestibulo-ocular reflex. I. Purkinje cell activity during visually guided horizontal smooth pursuit eye movements and passive head rotation. J Neurophysiol 41: 733–761
Mac Kay WA (1988) Cerebellar nuclear activity in relation to simple movements. Brain Res (in press)
Mano NI, Yamamoto K (1980) Simple spike activity of cerebellar Purkinje cells related to visually guided wrist tracking movements in the monkey. J Neurophysiol 43: 713–728
Mano NI, Yamamoto K (1982) Role of cerebellar Purkinje cells in voluntary limb movement. Exp Brain Res Suppl 6: 455–465
Marchetti E, Gauthier GM, Pellet J (1983) Cerebellar control of eye movements studied with injection of harmaline in the trained baboon. Arch Ital Biol 121: 1–17
Massion J (1973) Cervelet et mouvement. J Physiol (Paris) 67: 117–170
Mather JA, Lackner JR (1981) The influence of afferent, proprioceptive and timing factors on the accuracy of eye-hand tracking. Exp Brain Res 43: 406–412
Meyer GH, Lasker AG, Robinson DA (1985) The upper limit of human smooth pursuit velocity. Vision Res 25: 561–563
Noda H (1981) Visual mossy fiber inputs to the flocculus of the monkey. Ann N Y Acad Sci 374: 465–475
Noda H, Mikami A (1986) Discharges of neurons in the dorsal paraflocculus of monkeys during eye movements and visual stimulation. J Neurophysiol 56: 1129–1146
Noda H, Suzuki DA (1979) The role of the flocculus of the monkey in fixation and smooth pursuit eye movements. J Physiol (London) 294: 335–348
Oscarsson O (1969) Termination and functional organization of the dorsal spino-olivo-cerebellar path. J Physiol (London) 200: 129–149
Oscarsson O (1979) Functional units of the cerebellum sagittal zones and microzones. TINS June: 143–145
Paillard J (1971) Les determinants moteurs de l'organisation de 1'espace. Cah Psychologie 14: 261–316
Rashbass C (1961) The relationship between saccadic and smooth tracking eye movements. J Physiol (London) 159: 326–338
Riche D, Courville J, Massion J, Nieoullon A (1971) Anatomie stéréotaxique des noyaux cérébelleux du babouin. J Physiol (Paris) 63: 783–857
Rispal-Padel L, Cicirata F, Pons JC (1982) Cerebellar nuclear topography of simple and synergistic movements in the alert monkey. Exp Brain Res 47: 365–380
Rispal-Padel L, Cicirata F, Pons JC (1983) Neocerebellar synergies. Exp Brain Res Suppl 7: 213–223
Ritchie L (1976) Effects of cerebellar lesions on saccadic eye movements. J Neurophysiol 39: 1246–1256
Ron S, Robinson DA (1973) Eye movement evoked by cerebellar stimulation in the alert monkey. J Neurophysiol 16: 1011–1022
Rothenberg SJ, Selkoe D (1981a) Specific oculomotor deficit after diazepam. I. Saccadic eye movements. Psychopharmacology 74: 232–236
Rothenberg SJ, Selkoe D (1981b) Specific oculomotor deficit after diazepam. II. Smooth pursuit eye movements. Psychopharmacology 74: 237–240
Sato Y, Kawasaki T (1984) Functional localization in the three floccular zones related to eye movement control in the cat. Brain Res 290: 25–31
Sato Y, Yamamoto F, Shojaku H, Kawasaki T (1982) Neuronal pathway from floccular caudal zone contributing to vertical eye movements in cat. Role of group Y nucleus of vestibular nuclei. Brain Res 294: 375–380
Schalen L, Henriksson NG, Pyykko I (1982) Quantification of tracking eye movements in patients with neurological disorders. Acta Otolaryngol 93: 387–395
Schultz W, Montgomery EB, Marini R (1976) Stereotyped flexion of forelimb and hindlimb to microstimulations of dentate nucleus of the monkey. Brain Res 107: 152–155
Schultz W, Montgomery EB, Marini R (1979) Proximal limb movements in response to microstimulations of primate dentate and interpositus nuclei mediated by brain stem structure. Brain 102: 127–146
Schwarz DWF, Tomlinson RD (1977) Neuronal responses to eye muscle stretch in cerebellar lobule VI of the cat. Exp Brain Res 27: 101–111
Soechting JF, Ranish NA, Palminteri R, Terzuolo CA (1976) Changes in a motor pattern following cerebellar and olivary lesions in the squirrel monkey. Brain Res 105: 21–44
Stark L, Vossius G, Young LR (1962) Predictive control of eye tracking movements. IEEE Trans Human Fact Electron 3: 52–57
Steinbach MJ (1976) Pursuing the perceptual rather than the retinal stimulus. Vision Res 16: 1371–1376
Steinbach MJ, Held R (1968) Eye tracking of observer-generated target movement. Science 161: 187–188
Suzuki DA, Kase M, Noda H (1979) Visual and pursuit eye movement signal in the monkey vermis. Soc Neurosci Abstr 5: 107
Trouche E, Beaubaton D (1980) Initiation of a goal-directed movement in monkey. Role of the cerebellar dentate nucleus. Exp Brain Res 40: 311–321
Westheimer G (1954) Eye movement response to a horizontally moving visual stimulus. AMA Arch Ophthal 52: 932–941
Westheimer G, Blair SM (1973) Oculomotor defects in cerebellectomized monkeys. Invest Ophthalmol 12-8: 618–621
Westheimer G, Blair SM (1974) Functional organization of primate oculomotor system revealed by cerebellectomy. Exp Brain Res 21: 463–472
Yasui S, Young LR (1975) Perceived visual motion as effective stimulus to pursuit eye movement system. Science 190: 906–908
Zee DS, Yee RD, Cogan DC, Robinson DA, Engel WK (1976) Oculomotor abnormalities in hereditary cerebellar ataxia. Brain 99: 207–234
Zee DS, Yamazaki A, Butler PH, Gücer G (1981) Effects of ablation of flocculus and paraflocculus on eye movements in primate. J Neurophysiol 46: 878–899
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Vercher, J.L., Gauthier, G.M. Cerebellar involvement in the coordination control of the oculo-manual tracking system: effects of cerebellar dentate nucleus lesion. Exp Brain Res 73, 155–166 (1988). https://doi.org/10.1007/BF00279669
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DOI: https://doi.org/10.1007/BF00279669