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Role of primate basal ganglia and frontal cortex in the internal generation of movements

II. Movement-related activity in the anterior striatum

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Summary

In order to more comprehensively assess the role of the basal ganglia in the internal generation of movements, we studied the activity of neurons in the head of the caudate and in the rostral putamen in relation to the execution of movements. Monkeys performed self-initiated and stimulus-triggered arm reaching movements in separate blocks of trials. With stimulus-triggered movements, 217 striatal neurons increased their activity after the trigger stimulus (127 in caudate, 90 in putamen). Of these, 68 neurons showed time-locked responses to the trigger stimulus, with a median latency of 60 ms, that were independent of visual or auditory stimulus modalities. Three quarters of responses were conditional on a movement being performed. These responses may participate in neuronal processes through which the reception of a stimulus is translated into the execution of a behavioral reaction. Further, 44 neurons increased their activity before the earliest muscle activity without being clearly time-locked to the stimulus (148–324 ms before movement onset), 55 neurons were activated later before the movement, and 50 neurons were activated after movement onset. With self-initiated movements, 106 striatal neurons showed movement-related activity beginning up to 460 ms before movement onset (52 in caudate, 54 in putamen). Comparisons between the two types of movement were made on 53 neurons with premovement activity beginning more than 500 ms before self-initiated movements. Only one fifth of them also showed movement-related activity with stimulus-triggered movements, including trigger responses. Comparisons among 39 neurons with movement-related activity during self-initiated arm movements showed that about half of them also showed movement-related activity with stimulus-triggered movements. These data demonstrate a considerably segregated population of striatal neurons engaged in the internal generation of movements, whereas processes underlying the execution of movements appear to involve overlapping neuronal populations.

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References

  • Aldridge JW, Anderson RJ, Murphy JT (1980) The role of the basal ganglia in controlling a movement initiated by a visually presented cue. Brain Res 192: 3–16

    Google Scholar 

  • Amalric M, Condé H, Dormont JF, Farin D, Schmied A (1984) Activity of caudate neurons in cat performing a reaction time task. Neurosci Lett 49: 253–258

    Google Scholar 

  • Apicella P, Scarnati E, Schultz W (1991) Tonically discharging neurons of monkey striatum respond to preparatory and rewarding stimuli. Exp Brain Res 84: 672–675

    Google Scholar 

  • Boch RA, Goldberg ME (1989) Participation of prefrontal neurons in the preparation of visually guided eye movements in the rhesus monkey. J Neurophysiol 61: 1064–1084

    Google Scholar 

  • Chapman CE, Spidalieri G, Lamarre Y (1984) Discharge properties of area 5 neurons during arm movements triggered by sensory stimuli in the monkey. Brain Res 309: 63–77

    Google Scholar 

  • Chapman CE, Spidalieri G, Lamarre Y (1986) Activity of dentate neurons during arm movements triggered by visual, auditory, and somesthetic stimuli in the monkey. J Neurophysiol 55: 203–226

    Google Scholar 

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

    Google Scholar 

  • Crutcher MD, DeLong MR (1984b) Single cell studies of the primate putamen. II. Relations to direction of movement and pattern of muscular activity. Exp Brain Res 53: 244–258

    Google Scholar 

  • Davies J, Dray A (1976) Substance P in the substantia nigra. Brain Res 107: 623–627

    Google Scholar 

  • Evarts EV (1966) Pyramidal tract activity associated with a conditioned hand movement in the monkey. J Neurophysiol 29: 1011–1027

    Google Scholar 

  • Funahashi S (1983) Responses of monkey prefrontal neurons during a visual tracking task reinforced by substantia innominata self-stimulation. Brain Res 276: 267–276

    Google Scholar 

  • 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

    Google Scholar 

  • Gerfen CR (1984) The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311: 461–464

    CAS  PubMed  Google Scholar 

  • Godschalk M, Lemon RN, Nijs HGT, Kuypers HGJM (1981) Behaviour of neurones in monkey peri-arcuate and precentral cortex before and during visually guided arm and hand movements. Exp Brain Res 44: 113–116

    Google Scholar 

  • Graybiel AM, Ragsdale CW, Yoneoka ES, Elde RP (1981) An immunohistological study of enkephalins and other neuropeptides in the striatum of the cat with evidence that the opiate peptides are arranged to form mosaic patterns in register with the striosomal compartments visible by acetylcholinesterase staining. Neuroscience 6: 377–397

    Google Scholar 

  • Hikosaka O, Sakamoto M, Usui S (1989) Functional properties of monkey caudate neurons. II. Visual and auditory responses. J Neurophysiol 61: 799–813

    Google Scholar 

  • Ito SI (1982) Prefrontal unit activity of macaque monkeys during auditory and visual reaction time tasks. Brain Res 247: 39–47

    Google Scholar 

  • Kimura M (1990) Behaviorally contingent property of movement-related activity of the primate putamen. J Neurophysiol 63: 1277–1296

    Google Scholar 

  • Kimura M, Rajkowski J, Evarts E (1984) Tonically discharging putamen neurons exhibit set-dependent responses. Proc Natl Acad Sci USA 81: 4998–5001

    Google Scholar 

  • Kojima S (1980) Prefrontal unit activity in the monkey: relation to visual stimuli and movements. Exp Neurol 69: 110–123

    Google Scholar 

  • Kubota K, Hamada I (1978) Visual tracking and neuron activity in the post-arcuate area in monkeys. J Physiol (Paris) 74: 297–312

    Google Scholar 

  • Kurata K (1989) Distributions of neurons with set- and movement-related activity before hand and foot movements in the premotor cortex of rhesus monkeys. Exp Brain Res 77: 245–256

    Google Scholar 

  • Kurata K, Tanji J (1985) Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. II. Responses to movement triggering vs. nontriggering sensory signals. J Neurophysiol 53: 142–152

    Google Scholar 

  • Kurata K, Tanji J (1986) Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J Neurosci 6: 403–411

    Google Scholar 

  • Lamarre Y, Busby L, Spidalieri G (1983) Fast ballistic arm movements triggered by visual, auditory and somesthetic stimuli in the monkey. I. Activity of precentral cortical neurons. J Neurophysiol 50: 1343–1358

    Google Scholar 

  • Liles SL (1985) Activity of neurons in putamen during active and passive movements of the wrist. J Neurophysiol 53: 217–236

    Google Scholar 

  • Ljungberg T, Apicella P, Schultz W (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67: 145–163

    Google Scholar 

  • Mink JW, Thach WT (1991a) Basal ganglia motor control. I. Nonexclusive relation of pallidal discharge to five movement modes. J Neurophysiol 65: 273–300

    Google Scholar 

  • Mink JW, Thach WT (1991b) Basal ganglia motor control. II. Late pallidal timing relative to movement onset and inconsistent pallidal coding of movement parameters. J Neurophysiol 65: 301–329

    Google Scholar 

  • Montgomery EB Jr, Buchholz SR (1991) The striatum and motor cortex in motor initiation and execution. Brain Res 549: 222–229

    Google Scholar 

  • Mroz EA, Brownstein MJ, Leeman SE (1977) Evidence for substance P in the striato-nigral tract. Brain Res 125: 305–311

    Google Scholar 

  • Nambu A, Yoshida S, Jinnai K (1990) Discharge patterns of pallidal neurons with input from various cortical areas during movement in the monkey. Brain Res 519: 183–191

    Google Scholar 

  • Niki H (1974) Prefrontal unit activity during delayed alternation in the monkey. I. Relation to direction of response. Brain Res 68: 185–196

    Google Scholar 

  • Robinson DL, Goldberg ME, Stanton GB (1978) Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. J Neurophysiol 41: 910–932

    Google Scholar 

  • Rolls ET, Thorpe SJ, Maddison SP (1983) Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus. Behav Brain Res 7: 179–210

    Google Scholar 

  • Romo R, Schultz W (1987) Neuronal activity preceding self-initiated or externally timed arm movements in area 6 of monkey cortex. Exp Brain Res 67: 656–662

    Google Scholar 

  • Romo R, Schultz W (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. III. Neuronal activity in the supplementary motor area. Exp Brain Res 91: 396–407

    Google Scholar 

  • Sakai M (1974) Prefrontal unit activity during visually guided lever pressing reaction in the monkey. Brain Res 81: 297–309

    Google Scholar 

  • Sawaguchi T (1987) Properties of neuronal activity related to a visual reaction time task in the monkey prefrontal cortex. J Neurophysiol 58: 1080–1099

    Google Scholar 

  • Sawaguchi T, Matsumura M, Kubota K (1989) Depth distribution of neuronal activity related to a visual reaction time task in the monkey prefrontal cortex. J Neurophysiol 61: 435–446

    Google Scholar 

  • Schultz W (1986) Activity of pars reticulata neurons of monkey substantia nigra in relation to motor, sensory and complex events. J Neurophysiol 55: 660–677

    Google Scholar 

  • Schultz W (1989) Neurophysiology of basal ganglia. In: Calne DB (ed) Handbook of experimental pharmacology, vol 88, Springer, Berlin, Heidelberg New York, pp 1–45

    Google Scholar 

  • Schultz W, Romo R (1990) Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. J Neurophysiol 63: 607–624

    Google Scholar 

  • Schultz and Romo (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 

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

    Google Scholar 

  • Smith A (1979) The activity of supplementary motor area neurons during a maintained precision grip. Brain Res 172: 315–327

    Google Scholar 

  • Tanji J, Kurata K (1982) Comparison of movement-related activity in two motor cortical areas of primates. J Neurophysiol 48: 633–653

    Google Scholar 

  • Thorpe SJ, Rolls ET, Maddison S (1983) The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp Brain Res 49: 93–115

    Google Scholar 

  • Walker RJ, Kemp JA, Yajima H, Kitagawa K, Woodruff GN (1976) The action of substance P on mesencephalic reticular and substantia nigral neurones of the rat. Experientia 32: 214–215

    Google Scholar 

  • Watanabe M (1986) Prefrontal unit activity during delayed conditional go/no-go discrimination in the monkey. II. Relation to go and no-go responses. Brain Res 382: 15–27

    Google Scholar 

  • Weinrich M, Wise S (1982) The premotor cortex of the monkey. J Neurosci 2: 1329–1345

    CAS  PubMed  Google Scholar 

  • West MO, Carelli RM, Pomerantz M, Cohen SM, Gardner JP, Chapin JK, Woodward DJ (1990) A region in the dorsolateral striatum of the rat exhibiting single-unit correlations with specific locomotor limb movements. J Neurophysiol 64: 1233–1246

    Google Scholar 

  • Yin TCT, Mountcastle VB (1977) Visual input to the visuo-motor mechanisms of the monkey's parietal lobe. Science 197: 1381–1383

    Google Scholar 

Download references

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Author notes

  1. Ranulfo Romo

    Present address: Institute of Cellular Physiology, National Autonomous University of Mexico, Box 70-600, 04510, Mexico

  2. Eugenio Scarnati

    Present address: Laboratory of Human Physiology, School of Medicine, University of L'Aquila, L'Aquila, Italy

Authors and Affiliations

  1. Institut de Physiologie, Université de Fribourg, CH-1700, Fribourg, Switzerland

    Ranulfo Romo, Eugenio Scarnati & Wolfram Schultz

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  1. Ranulfo Romo
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  2. Eugenio Scarnati
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  3. Wolfram Schultz
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Romo, R., Scarnati, E. & Schultz, W. Role of primate basal ganglia and frontal cortex in the internal generation of movements. Exp Brain Res 91, 385–395 (1992). https://doi.org/10.1007/BF00227835

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  • DOI: https://doi.org/10.1007/BF00227835

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