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.
Similar content being viewed by others
References
Aggleton J, Passingham RE (1981) Stereotaxic surgery under X-ray guidance in the rhesus monkey, with special reference to the amygdala. Exp Brain Res 44:271–276
Alexander GE (1987) Selective neuronal discharge in monkey putamen reflects intended direction of planned limb movements. Exp Brain Res 67:623–634
Alexander GE, Delong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci 9:357–382
Canavan AGM (1986) Functions of the basal ganglia in man and monkey. Doctoral thesis. Oxford University
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 92:293–331
Crutcher MD, Delong MR (1984) Single cell studies of the primate putamen. Exp Brain Res 53:244–258
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, Bethesda
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 64–78
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 3:1586–1598
Goldman PS, Rosvold HE (1970) Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. Exp Neurol 27:291–304
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 77:212–220
Goldman-Rakic PS, Porrino LJ (1985) The primate mediodorsal nucleus and its projection to the frontal lobe. J Comp Neurol 242:535–560
Halsband U, Passingham RE (1985) Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis). Behav Brain Res 18:269–277
Hikosaka O, Sakamoto M (1986) Cell activity in monkey caudate nucleus preceding saccadic eye movements. Exp Brain Res 63:659–662
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 262:331–364
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 232:97–113
Jacobsen S, Butters N, Tovsky NJ (1978) Afferent and efferent subcortical projections of behaviorally defined sectors of prefrontal granular cortex. Brain Res 159:279–296
Jones E (1985) The thalamus. Plenum, New York
Kievit J, Kuypers HGJM (1977) Organization of the thalamocortical connections to the frontal lobe in the rhesus monkey. Exp Brain Res 29:299–322
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 169:263–290
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 15:185–234
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)
Miller WC, Mitchell SJ, Baker FH, Delong MR (1986) Instruction-dependent changes in neuronal activity in the primate globus pallidus. Soc Neurosci Abstr 12:207
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 274:213–224
Nambu A, Yoshida S, Jinnai K (1988) Projection on the motor cortex of thalamic neurons with pallidal input in the monkey. Exp Brain Res 71:658–662
Olszewski J (1952) The thalamus of Macaca mulatta. Karger, Basel
Passingham RE, Perry VH, Wilkinson F (1983) The long-term effects of removal of sensorimotor cortex in infant and adult rhesus monkeys. Brain 106:675–705
Passingham RE (1985) Premotor cortex: sensory cues and movement. Behav Brain Res 18:175–185
Passingham RE (1987) From where does the motor cortex get its instructions? In: Wise SP (ed) Higher brain functions. Wiley, New York, pp 67–97
Passingham RE (1988) Premotor cortex and preparation for movement. Exp Brain Res 70:590–596
Petrides M (1982) Motor conditional associative learning after selective prefrontal lesions in the monkey. Behav Brain Res 5:407–413
Preuss TM, Goldman-Rakic PS (1987) Crossed corticothalamic and thalamocortical connections of macaque prefrontal cortex. J Comp Neurol 257:269–281
Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor area. J Neurosci 4:559–560
Smith Y, Parent A (1986) Differential connections of caudate nucleus and putamen in the squirrel monkey. Neuroscience 18:347–371
Strick P (1985) How do the basal ganglia and cerebellum gain access to the cortical motor areas? Behav Brain Res 18:107–124
Yeterian EH, Pandya DN (1988) Corticothalamic connections of paralimbic regions in the rhesus monkey. J Comp Neurol 269:130–146
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Canavan, A.G.M., Nixon, P.D. & Passingham, R.E. Motor learning in monkeys (Macaca fascicularis) with lesions in motor thalamus. Exp Brain Res 77, 113–126 (1989). https://doi.org/10.1007/BF00250573
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00250573