Skip to main content
SpringerLink
Log in

The sensory guidance of movement: a comparison of the cerebellum and basal ganglia

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We used positron emission tomography (PET) to compare the contribution of the cerebellum and basal ganglia to the sensory guidance of movement. In one condition the subjects used a computer mouse to draw a series of lines on a computer screen (DRAW). In the second condition the same lines were presented to the subjects, and they had to track the lines with a mouse pointer on the screen (COPY). In a third condition the subjects were again presented with the same lines, and they simply followed movements of the pointer with their eyes (EYES). In the fourth condition, the subjects fixated a central point, ignoring the sequence of presented lines (FIX). The pons and cerebellum were activated more during visually guided tracking than in freely generated drawing (COPY vs DRAW). The basal ganglia were activated equally in both DRAW and COPY. The prefrontal and inferior temporal cortex were activated more when subjects drew lines freely (DRAW) than when they copied them (COPY). We conclude that the cerebellum is specialized for using sensory information to correct movements, but that the basal ganglia are involved both in movements that are self-generated and in movements that are guided by external cues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alexander GE (1987) Selective neuronal discharge in monkey putamen reflects intended direction of planned limb movements. Exp Brain Res 67:623–634

    Google Scholar 

  • Anderson TJ, Jenkins IH, Brooks DJ, Hawken MB, Frackowiak RSJ, Kennard C (1994) Cortical control of saccades and fixation in man: a PET study. Brain 117:1073–1084

    Google Scholar 

  • Berretta S, Perciavalle V, Poppele RE (1991) Origin of spinal projections to the anterior and posterior lobes of the rat cerebellum. J Comp Neurol 305:273–281

    Google Scholar 

  • Bosco G, Poppele RE (1993) Broad directional tuning in spinal projections to the cerebellum. J Neurophysiol 70:863–866

    Google Scholar 

  • Brooks DJ (1995) The role of the basal ganglia in motor control: contributions from PET. J Neurol Sci 128:1–13

    Google Scholar 

  • Buerger AA, Gross CG, Rocha-Miranda CE (1974) Effects of ventral putamen lesions on discrimination learning. J Comp Physiol Psychol 86:440–446

    Google Scholar 

  • Buswein E, Kolb FP, Leimbeck B, Rubia FJ (1983) Simple and compley spike activity of cerebellar Purkinje cells during active and pasive movements in the awake monkey. J Physiol (Lond) 339:379–394

    Google Scholar 

  • Connor NP, Abbs JH (1990) Sensorimotor contributions of the basal ganglia: recent advances. Phys Ther 70:864–872

    Google Scholar 

  • Crutcher MD, DeLong MR (1984) Single cell studies of the primate putamen. I. Functional organization. Exp Brain Res 53:233–243

    Google Scholar 

  • Deiber M-P, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RSJ (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84:393–402

    Google Scholar 

  • Flaherty AW, Graybiel AM (1993) Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey. J Neurosci 13:1120–1137

    Google Scholar 

  • Flowers KA (1976) Visual “closed loop” and “open loop” characteristics of voluntary movement in patients with Parkinsonism and intention tremor. Brain 99:269–310

    Google Scholar 

  • Flowers KA (1978) Lack of prediction in the motor behaviour of Parkinsonism. Brain 101:35–52

    Google Scholar 

  • Friston KJ, Passingham RE, Nutt JG, Heather JD, Sawle GV, Frackowiak RSJ (1989) Localisation in PET images: direct fitting of the intercommissural (AC-PC) line. J Cereb Blood Flow Metab 9:690–695

    Google Scholar 

  • Friston KJ, Frith CD, Liddle PF, Dolan RJ, Lammertsma AA, Frackowiak RSJ (1990) The relationship between global and local changes in PET scans. J Cereb Blood Flow Metab 10:458–466

    CAS  PubMed  Google Scholar 

  • Friston KJ, Frith CD, Liddle PF, Frackowiak RSJ (1991) Comparing functional (PET) images: the assessment of significant change. J Cereb Blood Flow Metab 11:690–699

    Google Scholar 

  • Frith CD, Friston K, Liddle PF, Frackowiak RS (1991) Willed action and the prefrontal cortex in man: a study with PET. Proc R Soc Lond B 244:241–246

    Google Scholar 

  • Glickstein M, May JG, Mercier RE (1985) Corticopontine projections in the macaque: the distribution of labelled cortical cells after large injections of horse-radish peroxidase in the pontine nuclei. J Comp Neurol 235:343–359

    Google Scholar 

  • Goldberg G (1985) Supplementary motor area structure and function: review and hypotheses. Exp Brain Res 8:567–588

    Google Scholar 

  • Grady CL, Maisog JM, Horwitz B, Ungerleider LG, Mentis MJ, Salerno J, Pietrini P, Wagner E, Haxby JV (1994) Age-related changes in cortical blood flow activation during visual processing of faces and location. J Neurosci 14:1450–1462

    Google Scholar 

  • Grafton ST, Mazziotta JC, Presty S, Friston KJ, Frackowiak RS, Phelps ME (1992) Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J Neurosci 12:2542–2548

    CAS  PubMed  Google Scholar 

  • Grafton ST, Woods RP, Tyszka M (1994) Functional imaging of procedural motor learning: relating cerebral blood flow with individual subject performance. Hum Brain Mapping 1:221–234

    Google Scholar 

  • Grill SE, Hallett M, Marcus C, McShane L (1994) Disturbances of kinaesthesia in patients with cerebellar disorders. Brain 117:1433–1447

    Google Scholar 

  • Hikosaka O, Wurtz RH (1983) Visual and oculomotor function of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade response. J Neurophysiol 49:1230–1253

    Google Scholar 

  • Hoesen G van, Yeterian EH, Lavizzo-Mourey R (1981) Widespread corticostriate projection from temporal cortex of the rhesus monkey. J Comp Neurol 199:205–219

    Google Scholar 

  • Ito M (1984) The cerebellum and neural content. Raven Press, New York

    Google Scholar 

  • Jahanshahi M, Jenkins IH, Passingham RE, Brown RG, Marsden CD, Brooks DJ (1995) The effect of context on volitional actions: evidence from recording movement-related potentials and measurement of regional cerebral blood flow with PET. Brain 118:913–933

    PubMed  Google Scholar 

  • Jenkins IH, Brooks DJ, Nixon PD, Frackowiak RSJ, Passingham RE (1994) Motor sequence learning: a study with positron emission tomography. J Neurosci 14:3775–3790

    Google Scholar 

  • Kolb FP, Rubia FJ, Bauswein E (1987) Cerebellar unit responses of the mossy fibre system to passive movements in the decerebrate cat. Exp Brain Res 68:234–248

    Google Scholar 

  • Lang W, Lang M, Podreka I, Steiner M, Uhl F, Suess E, Muller C, Deeke L (1988) DC-potential shifts and regional cerebral blood flow reveal frontal cortex involvement in human visuomotor learning. Exp Brain Res 71:353–364

    Google Scholar 

  • Lueck CJ, Tanyeri S, Crawford TJ, Henderson L, Kennard C (1990) Antisaccades and remembered saccades in Parkinson's disease. J Neurol Neurosurg Pschiatry 53:284–288

    Google Scholar 

  • Miall RC, Weir DJ, Stein JF (1987) Visuo-motor tracking during reversible inactivation of the cerebellum. Exp Brain Res 65:455–464

    Google Scholar 

  • Mikami A, Ito S, Fubota K (1982) Visual response properties of dorsolateral prefrontal cortex neurons during a visual fixation task. J Neurophysiol 47:593–605

    Google Scholar 

  • Murphy JT, MacKay WA, Johnson F (1973) Differences between cerebellar mossy and climbing fibre responses to natural stimulation of forelimb muscle proprioceptors. Brain Res 55:263–289

    Google Scholar 

  • Mushiake H, Strick PL (1993) Preferential activity of dentate neurons during limb movements guided by vision. J Neurophysiol 70:2660–2664

    Google Scholar 

  • Mushiake H, Strick PL (1995) Pallidal neuron activity during sequential arm movements. J Neurophysiol 74:2754–2759

    Google Scholar 

  • Ojakangas CL, Ebner TJ (1992) Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey. J Neurophysiol 68:2222–2236

    Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Passingham RE (1993) The frontal lobes and voluntary action. Oxford Science Publications, Oxford

    Google Scholar 

  • Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RSJ, Brooks DJ (1992) Impaired mesial frontal and putamen activation in Parkinson's disease: a PET study. Ann Neurol 32:151–161

    Google Scholar 

  • Romo R, Scarnati E, Schultz W (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. II. Movement-related activity in the anterior striatum. Exp Brain Res 91:385–395

    Google Scholar 

  • Saint-Cyr J, Ungerleider LG, Desimone R (1990) Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey. J Comp Neurol 298:129–156

    Google Scholar 

  • Schmahmann JD, Pandya DN (1989) Anatomical investigation of projections to the basis pontis from posterior parietal association cortices in rhesus monkey. J Comp Neurol 289:53–73

    Google Scholar 

  • Schmahmann JD, Pandya DN (1991) Projections to the basis pontis from the superior temporal sulcus and superior temporal region in the rhesus monkey. J Comp Neurol 308:224–248

    Google Scholar 

  • Schultz W, Romo R (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. I. Preparatory activity in the anterior striatum. Exp Brain Res 91:363–384

    Google Scholar 

  • Schwartz BA, Halgren E, Fuster J, Mandelkern M (1994) An 18FGD study of cortical activation during a short-term visual memory task in humans. Neuroreport 5:925–928

    Google Scholar 

  • Selemon LD, Goldman-Rakic PS (1985) Logitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci 5:776–794

    Google Scholar 

  • Seltzer B, Pandya DN (1994) Parietal, temporal, and occipital projections to the cortex of the superior temporal sulcus in the rhesus monkey: a retrograde tracer study. J Comp Neurol 343:445–463

    Google Scholar 

  • Spinks TJ, Jones T, Bailey DL, Townsend DW, Grootoonk S, Bloomfield PM, Gilardi M-C, Casey ME, Sipe B, Reed J (1992) Physical performance of a positron tomograph for brain imaging with retractable septa. Phys Med Biol 8:1637–1655

    Google Scholar 

  • Stein J, Miall RC, Weir D (1987) The role of the cerebellum in the visual guidance of movements. In: Glickstein M, Yeo C, Stein J (eds) Cerebellum and Neuronal Plasticity, Plenum, New York, pp 175–191

    Google Scholar 

  • Stein JF, Glickstein M (1992) Role of the cerebellum in visual guidance of movement. Physiol Rev 72:976–1015

    Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York

    Google Scholar 

  • Thach WT, Goodkin HP, Keating IG (1992) The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci 15:403–442

    Google Scholar 

  • Townsend DW, Geissbuhler A, Defrise M, Hoffmann EJ, Spinks TJ, Bailey DL, Gilardi M-C, Jones T (1991) Fully three-dimensional reconstruction for a PET camera with retractable septa. IEEE Trans Med Imaging 10:505–512

    Google Scholar 

  • Ungerleider LG, Desimone R, Galkin T, Mishkin M (1984) Subcortical projections of area MT in the macaque. J Comp Neurol 223:368–386

    Google Scholar 

  • Ungerleider LG, Gaffan D, Pelak VS (1989) Projections from inferotemporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys. Exp Brain Res 76:473–484

    Google Scholar 

  • Wichmann T, Bergman H, DeLong MR (1994) The primate subthalamic nucleus. J Functional properties in intact animals. J Neurophysiol 72:494–506

    Google Scholar 

  • Woods RP, Cherry SR, Mazziotta JC (1992) Rapid automated algorithm for aligning and reslicing PET images. J Comput Assist Tomogr 16:620–633

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. MRC Cyclotron Unit, Hammersmith Hospital, DuCane Road, W12 OHS, London, UK

    J. Jueptner, I. H. Jenkins, D. J. Brooks & R. E. Passingham

  2. Wellcome Department of Cognitive Neurology, Institute of Neurology, WC1N 3BG, London, UK

    M. Jueptner, R. S. J. Frackowiak & R. E. Passingham

  3. Department of Experimental Psychology, University of Oxford, South Parks Road, OX1 3UD, Oxford, UK

    R. E. Passingham

  4. Department of Neurology, University Clinics Essen, Hufelandstrasse 55, D-45122, Essen, Germany

    J. Jueptner

Authors
  1. J. Jueptner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Jueptner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. H. Jenkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. J. Brooks
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. S. J. Frackowiak
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. E. Passingham
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jueptner, J., Jueptner, M., Jenkins, I.H. et al. The sensory guidance of movement: a comparison of the cerebellum and basal ganglia. Exp Brain Res 112, 462–474 (1996). https://doi.org/10.1007/BF00227952

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227952

Key words

Search

Navigation