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Activity of neurons of the subthalamic nucleus in relation to motor performance in the cat

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Abstract

The activity of subthalamic nucleus neurons related to motor performance was studied in three unrestrained cats operantly conditioned to perform a lever-release movement. The movement was initiated either rapidly after the trigger stimulus (a brief sound) in a simple reaction-time paradigm or after a delay in trials identified by a tone cue. These paradigms were randomly presented. The activity of 171 neurons was recorded in the contralateral and in the ipsilateral subthalamic nucleus, with respect to the performing limb. The mean spontaneous activity of cells in the ipsilateral side (18.5±13.8 imp/s, mean±SD) was higher than that in the contralateral side (8.5±8.1 imp/s). A total of 145 cells (85%) presented significant changes in activity in relation to the lever-release movement (task-related cells). The remaining 26 cells were either related to other events of the task (n=15; lever-press or reinforcement occurrence) or not related at all to the task performance (n=11). The majority of changes of activity of task-related cells were initial increases in discharge, which started on average, 127 ms before movement onset and lasted several hundreds of milliseconds. These increases in discharge were more frequent in the contralateral side (75 of 80 task-related cells, 94%) than in the ipsilateral side (43 of 65 task-related cells, 66%). The changes in activity, either increases or decreases, occurred early after the trigger stimulus, since 62% of them had a latency of less than 100 ms. Although the mean latency of initial increases was rather similar in both sides (97 ms contralateral versus 104 ms ipsilateral), the contralateral side was characterized by a high proportion of very early responses (less than 20 ms). For most neurons, the early changes in activity described above were absent after the trigger stimulus in the delayed condition. For certain neurons, the changes in activity prior to movement were different in reactiontime condition and in delayed condition, showing that the pattern of activity preceding movement might depend on the temporal requirements for motor initiation. The results suggest that a significant proportion of subthalamic cells are involved in the preparation and the initiation phases of the lever-release movement studied, although other hypotheses (e.g. stimulus-related responses) cannot be definitely ruled out. The timings and patterns of the changes in activity observed in the subthalamic nucleus in the present study, and in the pallidal complex previously, cannot be explained easily by the classical scheme where the external pallidum inhibits the subthalamic nucleus. The results suggest rather that the subthalamic nucleus, driven by a yet-to-be-determined excitatory input, exerts an excitatory influence on the pallidum and plays a crucial role in the control of the basal ganglia output neurons.

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References

  • Afsharpour S (1985) Topographical projections of the cerebral cortex to the subthalamic nucleus. J Comp Neurol 236: 14–28

    Google Scholar 

  • Albin RL, Aldridge W, Young AB, Gilman S (1989) Feline subthalamic nucleus neurons contain glutamate-like but not GABA-like or glycine-like immunoreactivity. Brain Res 491: 185–188

    Google Scholar 

  • Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13: 266–271

    Article  CAS  PubMed  Google Scholar 

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9: 357–381

    Article  CAS  PubMed  Google Scholar 

  • Amalric M, Farm D, Dormont JF, Schmied A (1994) GABA receptors activation in the globus pallidus and entopeduncular nucleus: opposite effects on reaction time performance in the cat. Exp Brain Res 102: 244–258

    Google Scholar 

  • Anderson ME, Turner RS (1991) Activity of neurons in cerebellar-receiving and pallidal receiving areas of the thalamus of the behaving monkey. J Neurophysiol 66: 879–893

    Google Scholar 

  • Aziz TZ, Peggs D, Sambrook MA, Crossman AR (1991) Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phe-nyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism in the primate. Mov Disorders 6: 288–292

    Google Scholar 

  • Beckstead RM (1983) A reciprocal axonal connection between the subthalamic nucleus and the neostriatum in the cat. Brain Res 275: 137–142

    Google Scholar 

  • Bergman H, Wichmann T, DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249: 1436–1438

    CAS  PubMed  Google Scholar 

  • Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72: 507–520

    CAS  PubMed  Google Scholar 

  • Canteras NS, Shammah-Lagnado SJ, Silva SL, Ricardo AJ, Ricardo S (1990) Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res 513: 43–59

    Google Scholar 

  • 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: 293–332

    Google Scholar 

  • Carpenter MB, Fraser RAR, Shriver JE (1968) The organization of the pallidosubthalamic fibers in the monkey. Brain Res 11: 522–559

    Google Scholar 

  • Carpenter MB, Carleton SC, Keller JT, Conte P (1981a) Connections of the subthalamic nucleus in the monkey. Brain Res 224: 1–29

    Google Scholar 

  • Carpenter MB, Batton RR, Carleton SC, Keller JT (1981b) Interconnections and organization of pallidal and subthalamic neurons in the monkey. J Comp Neurol 197: 579–603

    Google Scholar 

  • Cheruel F, Farin D, Dormont JF (1992) Rôle du noyau subthalamique dans la commande motrice (abstract). Premier colloque de la société des neurosciences, Strasbourg 1992. F20: 198, Soc. des Neurosciences, Bordeaux

  • Cheruel F, Dormont JF, Amalric M, Schmied A, Farin D (1994) The role of putamen and pallidum in motor initiation in the cat. I. Timing of movement-related single unit activity. Exp Brain Res 100: 250–266

    Google Scholar 

  • Crossman AR, Sambrook MA, Jackson A (1984) Experimental hemichorea/hemiballismus in the monkey. Brain 107: 579–596

    Google Scholar 

  • De Long MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13: 281–285

    Article  CAS  PubMed  Google Scholar 

  • DeLong MR, Crutcher MD, Georgopoulos AP (1985) Primate globus pallidus and subthalamic nucleus: functional organization. J Neurophysiol 53: 530–543

    Google Scholar 

  • De Vito JL, Anderson ME (1982) An autoradiographic study of efferent connections of the globus pallidus in Macaca mulatta. Exp Brain Res 46: 107–117

    Google Scholar 

  • Dormont JF, Farin D, Schmied A, Amalric M (1989) Cat red nucleus activity preceding movement depends on initiation conditions. Exp Brain Res 77: 271–282

    Google Scholar 

  • Fetz EE, Cheney PD (1980) Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J Neurophysiol 44: 751–772

    Google Scholar 

  • Filion M, Hébert R (1983) Redundancy in ascending and descending pathways mediating head turning elicited by entopenduncular stimulation in the cat. Neuroscience 10: 169–176

    Google Scholar 

  • Filion M, Tremblay L (1991) Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 547: 142–151

    Google Scholar 

  • Fujimoto K, Kita H (1993) Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res 609: 185–192

    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 

  • Ghez C, Vicario D (1978a) Discharge of red nucleus during voluntary muscle contraction: activity patterns and correlations with isometric force. J Phyiol (Paris) 74: 283–286

    Google Scholar 

  • Ghez C, Vicario D (1978b) The control of rapid limb movement in the cat. I. Response latency. Exp Brain Res 38: 321–331

    Google Scholar 

  • Groenewegen HJ, Berendse HW (1990) Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol. 294: 607–622

    CAS  PubMed  Google Scholar 

  • Hamada I, De Long MR (1992a) Excitotoxic acid lesions of the primate subthalamic nucleus result in reduced pallidal neuronal activity during active holding. J Neurophysiol 68: 1859–1866

    Google Scholar 

  • Hamada I, De Long MR (1992b) Excitotoxic acid lesions of the primate subthalamic nucleus result in transient dyskinesias of the contralateral limbs. J Neurophysiol 68: 1850–1858

    Google Scholar 

  • Hammond C, Deniau JM, Rizk A, Féger J (1978) Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res 151: 235–244

    Google Scholar 

  • Hartmann-von Monakow K, Akert K, Künzle H (1978) Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthlamic nucleus in the monkey. Exp Brain Res 33: 395–403

    Google Scholar 

  • Hazrati LN, Parent A (1992) Differential patterns of arborization of striatal and subthalamic fibers in the two pallidal segments in primates. Brain Res 598: 311–315

    Google Scholar 

  • Hazrati LN, Parent A, Mitchell S, Haber SN (1990) Evidence for interconnections between the two segments of the glopus pall-idus in primates: a PHA-L anterograde tracing study. Brain Res 533: 171–175

    Google Scholar 

  • Ilinsky IA, Kultas-Ilinsky K (1984) An autoradiographic study of topographical relationships between pallidal and cerebellar projections to the cat thalamus. Exp Brain Res 54: 95–106

    Google Scholar 

  • Jinnai K, Nambu A, Yoshida S (1987) Thalamic afferents to layer I of anterior sigmoid cortex originating from the VA-VL neurons with entopuncular input. Exp Brain Res 69: 67–76

    Google Scholar 

  • Kim R, Nakano K, Jayaraman K, Carpenter MB (1976) Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey. J Comp Neurol 169: 263–289

    Google Scholar 

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

    Google Scholar 

  • Kimura M, Aosaki T, Hu Y, Ishida A, Watanabe K (1992) Activity of primate putamen neuron is selective to the mode of voluntary movement: visually guided, self-initiated or memory guided. Exp Brain Res 89: 473–477

    CAS  PubMed  Google Scholar 

  • Kita H, Chang HT, Kitai ST (1983) Pallidal inputs to subthalamus:intracellular analysis. Brain Res 264: 255–265

    Google Scholar 

  • Kitai ST, Deniau JM (1981) Cortical inputs to the subthalamus: intracellular analysis. Brain Res 214: 411–415

    Google Scholar 

  • Kitai ST, Kita H (1987) Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia. In: Carpenter MB, Jaraman A (eds) The basal ganglia. II. Structure and function: current concepts. Plenum, New York, pp 357–373

    Google Scholar 

  • Künzle H (1977) Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp Brain Res 30: 481–492

    Google Scholar 

  • Luschei E, Saslow Carol, Glickstein M (1967) Muscle potentials in reaction time. Exp Neurol 18: 429–442

    Google Scholar 

  • Matsumura M, Kojima J, Gardiner TW, Hikosaka O (1992a) Visual and oculomotor functions of monkey subthalamic nucleus. J Neurophysiol 67: 1615–1632

    Google Scholar 

  • Matsumura M, Sawaguchi T, Kubota K (1992b) GABAergic inhibition of neuronal activity in the primate motor and premotor cortex during voluntary movement. J Neurophysiol 68: 692–702

    Google Scholar 

  • Miller WC, De Long MR (1987) Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model parkinsonism. In: Carpenter MB, Jayaraman A (eds) The basal ganglia, II. Plenum, New York, pp 415–427

    Google Scholar 

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

    Google Scholar 

  • Mitchell IJ, Jackson A, Sambrook MA, Crossman AR (1985) Common neural mechanisms in experimental chorea and hemiballismus in the monkey. Evidence from 2-deoxyglucose autoradiography. Brain Res 339: 346–350

    Google Scholar 

  • Mitchell IJ, Jackson A, Sambrook MA, Crossman AR (1989) The role of the subthalamic nucleus in experimental chorea. Evidence from 2-deoxyglucose metabolic mapping and horseradish peroxydase tracing studies. Brain 112: 1533–1548

    Google Scholar 

  • Moriizumi T, Nakamura Y, Kitao Y, Kudo M (1987) Ultrastructural analyses of afferent terminals in the subthalamic nucleus of the cat with a combined degeneration and horseradish peroxidase tracing method. J Comp Neurol 265: 159–174

    Google Scholar 

  • Mouroux M, Féger J (1993) Evidence that the parafascicular projection to the subthalamic nucleus is glutamatergic. Neuroreport 4, 613–615

    Google Scholar 

  • Nakanishi H, Kita H, Kitai ST (1987) Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res 437: 45–55

    Google Scholar 

  • Nauta HJW, Cole M (1978) Efferent projections of the subthalamic nucleus: an autoradiographic study in monkey and cat. J Comp Neurol 180: 1–16

    Google Scholar 

  • Palombo E, Porrino LJ, Bankiewicz KS, Crane AM, Sokoloff L, Kopin IJ (1990) Local cerebral glucose utilization in monkeys with hemiparkinsonism induced by intracarotid infusion of the neurotoxin MPTP. J Neurosci 10: 860–869

    Google Scholar 

  • Parent A (1990) Extrinsic connections of the basal ganglia. Trends Neurosci 13: 254–258

    Google Scholar 

  • Parent A, Hazrati LN (1993) Anatomical aspects of information processing in primate basal ganslia. Trends Neurosci 16: 111–116

    Google Scholar 

  • Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Rev 20: 128–154

    Article  CAS  PubMed  Google Scholar 

  • Parent A, Smith Y (1987) Organization of efferent projections of the subthalamic nucleus in the squirrel monkey as revealed by retrograde labeling methods. Brain Res 436: 296–310

    Google Scholar 

  • Percheron G, Yelnik J, François C (1984) A golgi analysis of the primate globus pallidus. III. Spatial organization of the striatopallidal complex. J Comp Neurol 227: 214–227

    Google Scholar 

  • Petras JM (1969) Some efferent connections of the motor and somatosensory cortex of simian primates and felid, canid and procyonid carnivores. Ann NY Acad Sci 167: 469–505

    Google Scholar 

  • Price RH Jr, Hollingsworth Z, Young AB, Penney JB Jr (1993) Excitatory amino acid receptor regulation after subthalamic nucleus lesions in the rat. Brain Res 602: 157–160

    Google Scholar 

  • Rinvik E, Grofova I, Hammond C, Féger J, Deniau JM (1979) A study of the afferent connections to the subthalamic nucleus in the monkey and the cat using the HRP technique. Adv Neurol 24: 53–70

    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 

  • Rouzaire-Dubois B, Scarnati E (1985) Bilateral corticosubthalamic nucleus projections: an electrophysiological study in rats with chronic cerebral lesions. Neurosci 15: 69–79

    Google Scholar 

  • Schmied A, Bénita M, Condé H, Dormont JF (1979) Activity of ventrolateral thalamic neurons in relation to a simple reaction time task in the cat. Exp Brain Res 36: 285–300

    Google Scholar 

  • Sellal F, Hirsch E, Lisovoski F, Mutschler V, Collard M, Marescaux C (1992) Contralateral disappearance of parkinsonian signs after subthalamic hematoma. Neurology 42: 255–256

    Google Scholar 

  • Smith Y, Parent A (1988) Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreativity. Brain Res 453: 353–356

    Google Scholar 

  • Smith Y, Bolam JP, Von Krosigk M (1990a) Topographical and synaptic organization of the gaba-containing pallidosubthalamic projection in the rat. Eur J Neurosci 2: 500–511

    Google Scholar 

  • Smith Y, Hazrati LN, Parent A (1990b) Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J Comp Neurol 294: 306–323

    Google Scholar 

  • Sugimoto T, Hattori T, Mizuno N, Itoh K, Sato M (1983) Direct projections from the centre median-parafascicular complex to the subthalamic nucleus in the cat and rat. J Comp Neurol 214: 209–216

    Google Scholar 

  • Tremblay L, Filion M, Bédard JP (1989) Responses of pallidal neurons to striatal stimulation in monkeys with MPTP-induced parkinsonism. Brain Res 498: 17–33

    Google Scholar 

  • Turski L, Klockgether T, Turski WA, Schwarz M, Sontag KH (1990) The entopeduncular nucleus regulates muscle tone in genetically spastic rats: role of substance P and γ-aminobutyric acid. Brain Res 509: 347–350

    Google Scholar 

  • Uno M, Yoshida M (1975) Monosynaptic inhibition of thalamic neurons produced by stimulation of the pallidal nucleus in cats. Brain Res 99: 377–380

    Google Scholar 

  • Vicario DS, Martin JH, Ghez C (1983) Specialized subregions in the cat motor cortex: a single unit analysis in the behaving animal. Exp Brain Res 51: 351–367

    Google Scholar 

  • Whittier JR (1947) Ballism and the subthalamic nucleus (nucleus hypothalamicus; corpus luysii). Review of the literature and study of thirty cases. Arch Neurol Psychol 6: 672–692

    Google Scholar 

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

    Google Scholar 

  • Wichmann T, Bergman H, De Long MR (1994b) The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 72: 521–530

    CAS  PubMed  Google Scholar 

  • Yamamoto T, Noda T, Miyata M, Nishimura Y (1984) Electrophysiological and morphological studies on thalamic neurons receiving entopedunculo- and cerebello-thalamic projections in the cat. Brain Res 301: 231–242

    Google Scholar 

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  1. Laboratoire de Neurobiologie et Neuropharmacologie du Développement, CNRS URA 1121, Université de Paris-Sud, Bât. 440, F-91405, Orsay Cedex, France

    F. Cheruel, J. F. Dormont & D. Farin

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Cheruel, F., Dormont, J.F. & Farin, D. Activity of neurons of the subthalamic nucleus in relation to motor performance in the cat. Exp Brain Res 108, 206–220 (1996). https://doi.org/10.1007/BF00228095

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