Experimental Brain Research

, Volume 77, Issue 1, pp 113–126 | Cite as

Motor learning in monkeys (Macaca fascicularis) with lesions in motor thalamus

  • A. G. M. Canavan
  • P. D. Nixon
  • R. E. Passingham
Article

Summary

The study examines the nature of the influence that the basal ganglia exert on frontal cortex via the motor nuclei of the thalamus. Twelve monkeys were trained to pull a handle given one colour cue and to turn it given another. Bilateral lesions were then placed in the ventral thalamus. Four monkeys with large anterior lesions including the VA nucleus and the anterior part of VLo were severely impaired at relearning the task. Monkeys with small lesions in VAmc or with lesions centred on VLo were not impaired. The analysis of the histology suggests that the impairment in the four monkeys did not result from involvement of the cerebellar relay through nucleus X. It is argued that the animals are not impaired because of faulty execution. This suggests that the basal ganglia have an influence on motor learning.

Key words

Thalamus Basal ganglia Motor learning Akinesia Monkey 

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References

  1. Aggleton J, Passingham RE (1981) Stereotaxic surgery under X-ray guidance in the rhesus monkey, with special reference to the amygdala. Exp Brain Res 44:271–276Google Scholar
  2. Alexander GE (1987) Selective neuronal discharge in monkey putamen reflects intended direction of planned limb movements. Exp Brain Res 67:623–634Google Scholar
  3. Alexander GE, Delong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci 9:357–382Google Scholar
  4. Canavan AGM (1986) Functions of the basal ganglia in man and monkey. Doctoral thesis. Oxford UniversityGoogle Scholar
  5. Carpenter MB, Whittier JR, Mettler FA (1950) Analysis of choreoid hyperkinesia in the rhesus monkey: surgical and pharmacological analysis of hyperkinesia resulting from lesions in the subthalamic nucleus of Luys. J Comp Neurol 92:293–331Google Scholar
  6. Crutcher MD, Delong MR (1984) Single cell studies of the primate putamen. Exp Brain Res 53:244–258Google Scholar
  7. Delong MR, Georgopoulos AP (1981) Motor function of the basal ganglia. In: Brookhart JM, Mountcastle VB, Brooks VB (eds) Handbook of physiology: the nervous system, Vol II. Motor control, Part 1. American Physiological Society, BethesdaGoogle Scholar
  8. Delong MR, Georgopoulos AP, Crutcher MD (1984) Functional organization of the basal ganglia: contribution of single-cell recording studies. In: Evarts EV (ed) Functions of the basal ganglia. CIBA symposium 107. Pitman, London, pp 64–78Google Scholar
  9. Georgopoulos AP, Delong MR, Crutcher MD (1983) Relations between parameters of step-tracking movements and single-cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey. J Neurosci 3:1586–1598Google Scholar
  10. Goldman PS, Rosvold HE (1970) Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. Exp Neurol 27:291–304Google Scholar
  11. Goldman PS, Rosvold HE, Vest B, Galkin TW (1971) Analysis of the delayed-alternation defecit produced by dorsolateral prefrontal lesions in the rhesus monkey. J Comp Physiol Psychol 77:212–220Google Scholar
  12. Goldman-Rakic PS, Porrino LJ (1985) The primate mediodorsal nucleus and its projection to the frontal lobe. J Comp Neurol 242:535–560Google Scholar
  13. Halsband U, Passingham RE (1985) Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis). Behav Brain Res 18:269–277Google Scholar
  14. Hikosaka O, Sakamoto M (1986) Cell activity in monkey caudate nucleus preceding saccadic eye movements. Exp Brain Res 63:659–662Google Scholar
  15. Ilinsky IA, Kultas-Ilinsky K (1987) Sagittal cytoarchitectonic maps of the Macaca mulatta thalamus with a revised nomenclature of the motor-related nuclei validated by observations on their connectivity. J Comp Neurol 262:331–364Google Scholar
  16. Isseroff A, Rosvold HE, Galkin JW, Goldman-Rakic PS (1982) Spatial memory impairment following damage to the mediodorsal nucleus of the thalamus in rhesus monkeys. Brain Res 232:97–113Google Scholar
  17. Jacobsen S, Butters N, Tovsky NJ (1978) Afferent and efferent subcortical projections of behaviorally defined sectors of prefrontal granular cortex. Brain Res 159:279–296Google Scholar
  18. Jones E (1985) The thalamus. Plenum, New YorkGoogle Scholar
  19. Kievit J, Kuypers HGJM (1977) Organization of the thalamocortical connections to the frontal lobe in the rhesus monkey. Exp Brain Res 29:299–322Google Scholar
  20. Kim R, Nakano K, Jayaraman A, Carpenter MB (1976) Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey. J Comp Neurol 169:263–290Google Scholar
  21. Kunzle H (1978) An autoradiographic analyis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in Macaca fascicularis. Brain Behav Evol 15:185–234PubMedGoogle Scholar
  22. Matelli W, Luppino G, Fogassi L, Rizzolatti G (1989) Thalamic input to inferior area 6 and area 4 in the macaque monkey. J Comp Neurol (in press)Google Scholar
  23. Miller WC, Mitchell SJ, Baker FH, Delong MR (1986) Instruction-dependent changes in neuronal activity in the primate globus pallidus. Soc Neurosci Abstr 12:207Google Scholar
  24. Miyata M, Sasaki K (1984) Horseradish peroxidase studies on thalamic and striatal connections of the mesial part of area 6 in the monkey. Brain Res 274:213–224Google Scholar
  25. Nambu A, Yoshida S, Jinnai K (1988) Projection on the motor cortex of thalamic neurons with pallidal input in the monkey. Exp Brain Res 71:658–662Google Scholar
  26. Olszewski J (1952) The thalamus of Macaca mulatta. Karger, BaselGoogle Scholar
  27. Passingham RE, Perry VH, Wilkinson F (1983) The long-term effects of removal of sensorimotor cortex in infant and adult rhesus monkeys. Brain 106:675–705Google Scholar
  28. Passingham RE (1985) Premotor cortex: sensory cues and movement. Behav Brain Res 18:175–185Google Scholar
  29. Passingham RE (1987) From where does the motor cortex get its instructions? In: Wise SP (ed) Higher brain functions. Wiley, New York, pp 67–97Google Scholar
  30. Passingham RE (1988) Premotor cortex and preparation for movement. Exp Brain Res 70:590–596Google Scholar
  31. Petrides M (1982) Motor conditional associative learning after selective prefrontal lesions in the monkey. Behav Brain Res 5:407–413Google Scholar
  32. Preuss TM, Goldman-Rakic PS (1987) Crossed corticothalamic and thalamocortical connections of macaque prefrontal cortex. J Comp Neurol 257:269–281Google Scholar
  33. Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor area. J Neurosci 4:559–560Google Scholar
  34. Smith Y, Parent A (1986) Differential connections of caudate nucleus and putamen in the squirrel monkey. Neuroscience 18:347–371Google Scholar
  35. Strick P (1985) How do the basal ganglia and cerebellum gain access to the cortical motor areas? Behav Brain Res 18:107–124Google Scholar
  36. Yeterian EH, Pandya DN (1988) Corticothalamic connections of paralimbic regions in the rhesus monkey. J Comp Neurol 269:130–146Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • A. G. M. Canavan
    • 1
    • 2
  • P. D. Nixon
    • 1
    • 2
  • R. E. Passingham
    • 1
    • 2
  1. 1.Psychologisches InstitutTübingenFederal Republic of Germany
  2. 2.Department of Experimental PsychologyUniversity of OxfordOxfordUK

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