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The activity of pars compacta neurons of the monkey substantia nigra in relation to motor activation

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Summary

The extracellular activity of single pars compacta neurons of the substantia nigra was recorded in awake monkeys. Animals were subjected to a behavioral paradigm consisting of separate phases of preparation for trained movements and their execution. Cell activity was also studied during untrained movements.

Two basic firing patterns could be distinguished in the substantia nigra, depending on the subdivision examined. Pars compacta neurons at rest discharged impulses 1.0 to 2.0 ms in duration at a rate of 0 to 8/s, contrasting with the shorter pars reticulata discharges (0.6 to 1.0 ms long) occurring at higher frequencies (30 to 110 impulses/s). Forty of 68 tested and histologically-localized pars compacta neurons significantly changed, mostly increased, their discharge rate during and sometimes before the execution of trained or untrained individual large reaching movements of the contralateral arm. Distal movements of the arm or postural adjustments did not lead to detectable changes. Only a minority of these neurons showed modulated activity prior to onset of movement. None of the neurons responded to the sensory cues of moderate intensity employed in the paradigm.

The modulations were of a slow and moderate nature but were reproducible from trial to trial. Peak frequencies never exceeded 20 impulses/s. The duration of altered activity in many cells exceeded that of the arm movements. These characteristics thus contrasted with the more dramatic electromyographic changes of the involved muscles.

Sixteen of 23 neurons lying dorsally to the substantia nigra with electrophysiological characteristics similar to pars compacta neurons were modulated in the same fashion during performance in the paradigm.

We conclude that the activity of nigral pars compacta neurons is modulated in relation to motor activation. They do not appear to encode detailed movement parameters, rather they may subserve a more general function that is associated with behavioral, particularly motor, activation.

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References

  • Bernheimer H, Birkmayer W, Hornykiewicz O, Zellinger K, Seitelberger F (1973) Brain dopamine and the syndromes of Parkinson and Huntington: clinical, morphological and neurochemical correlations. J Neurol Sci 20: 415–455

    Article  CAS  PubMed  Google Scholar 

  • Bishop PO, Burke W, Davis R (1962) The identification of single units in central visual pathways. J Physiol (Lond) 162: 409–431

    Google Scholar 

  • Bogerts B (1981) A brainstem atlas of catecholaminergic neurons in man, using melanin as a natural marker. J Comp Neurol 197: 63–80

    Google Scholar 

  • Bunney BS, Aghajanian GK, Roth RH (1973) Comparison of effects of L-DOPA, amphetamine and apomorphine on firing rate of rat dopaminergic neurons. Nature New Biol 245: 123–125

    Google Scholar 

  • Chiodo LA, Antelmann SM, Caggiula AR, Lineberry CG (1980) Sensory stimuli alter the discharge rate of dopamine (DA) neurons: evidence for two functional types of DA cells in the substantia nigra. Brain Res 189: 544–549

    Google Scholar 

  • DeLong M, Georgopoulos A (1979) Motor functions of the basal ganglia as revealed by studies of single cell activity in the behaving primate. Adv Neurol 24: 131–140

    Google Scholar 

  • DiCarlo V, Hubbard JE, Pate P (1973) Fluorescence histochemistry of monoamine-containing cell bodies in the brain stem of the squirrel monkey (Saimiri sciureus). IV. An atlas. J Comp Neurol 152: 347–372

    Google Scholar 

  • Ehringer H, Hornykiewicz O (1960) Verteilung von Noradrenalin und Dopamin (3-Hydroxytyramin) im Gehirn des Menschen und ihr Verhalten bei Erkrankungen des extrapyramidalen Systems. Klin Wochenschr 38: 1236–1239

    Google Scholar 

  • Emmett-Oglesby MW, Lewy AJ, Albert LH, Seiden LS (1978) Role of lever responding and water presentation in altering rat brain catecholamine metabolism. J Pharm Exp Ther 204: 406–415

    Google Scholar 

  • Evarts EV, Teräväinen H, Calne DB (1981) Reaction time in Parkinson's disease. Brain 104: 167–186

    CAS  PubMed  Google Scholar 

  • Fabre M, Rolls ET, Ashton JP (1982) Neuronal activity in the region of the ventral tegmental area and substantia nigra related to the initiation of behavioural responses. Neurosci Lett [Suppl] 10: S168

    Google Scholar 

  • Francois C, Percheron G, Yelnik J, Heyner S (1981) The subdivisions of the macaque substantia nigra in stereotaxic ventricular coordinates. Neurosci Lett [Suppl] 7: S129

    Google Scholar 

  • Garver DL, Sladeck JR (1975) Monoamine distribution in primate brain. I. Catecholamine-containing perikarya in the brainstem of Macaca speciosa. J Comp Neurol 159: 289–304

    Google Scholar 

  • Goldstein M, Battista AF, Ohmoto T, Anagnoste B, Fuxe K (1973) Tremor and involuntary movements in monkeys: effect of L-Dopa and of a dopamine receptor stimulating agent. Science 179: 816–817

    Google Scholar 

  • Graybiel AM, Ragsdale CW (1979) Fiber connections of the basal ganglia. In: Cuénod M, Kreutzberg GW, Bloom FE (eds) Development and chemical specificity of neurons. Elsevier, Amsterdam, pp 239–283

    Google Scholar 

  • Gross C, Féger J, Seal J, Haramburu P, Bioulac B (1983) Neuronal activity in area 4 and movement parameters recorded in trained monkeys after unilateral lesion of the substantia nigra. Exp Brain Res [Suppl] 7: 181–193

    Google Scholar 

  • Guyenet PG, Aghajanian GK (1978) Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra. Brain Res 150: 69–84

    Google Scholar 

  • Hellweg FC, Schultz W, Creutzfeldt O (1977) Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation. J Neurophysiol 40: 462–479

    Google Scholar 

  • Hikosaka O, Wurtz RH (1981) The role of the substantia nigra in the initiation of saccadic eye movements. In: Fuchs AF, Becker B (eds) Progress in oculo-motor research. Elsevier, Amsterdam, pp 145–152

    Google Scholar 

  • Hommer DW, Bunney BS (1980) Effect of sensory stimuli on the activity of dopaminergic neurons: involvement of nondopaminergic nigral neurons and striato-nigral pathways. Life Sci 27: 377–386

    Google Scholar 

  • Jacobowitz DM, MacLean PD (1978) A brainstem atlas of catecholaminergic neurons and serotoninergic perikarya in a pygmy primate (Cebuella pygmaea). J Comp Neurol 177: 397–416

    Google Scholar 

  • Joseph JP, Boussaoud D (1982) Involvement of th substantia nigra pars reticulata in eye-and-head movements in the cat. Neurosci Lett [Suppl] 10: S257

    Google Scholar 

  • Lindsay WS, Herndon JG, Blakely RD, Justice JB, Neill DB (1981) Voltammetric recording from neostriatum from behaving monkey. Brain Res 220: 391–396

    Google Scholar 

  • Merrill EG, Ainsworth A (1972) Glass-coated platinum-plated tungsten microelectrodes. Med Biol Eng 10: 662–672

    Google Scholar 

  • Miller JD, Sanghera MK, German DC (1981) Mesencephalic dopaminergic unit activity in the behaviorally conditioned rat. Life Sci 29: 1255–1263

    Google Scholar 

  • Mora F, Mogenson GJ, Rolls ET (1977) Activity of neurons in the region of the substantia nigra during feeding in the monkey. Brain Res 133: 267–276

    Google Scholar 

  • Mountcastle VB, Talbot WH, Sakata H, Hyvärinen J (1969) Cortical neuronal mechanisms in flutter-vibration studied in unanaesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol 32: 452–484

    Google Scholar 

  • Nieoullon A, Chéramy A, Glowinski J (1978) Release of dopamine evoked by electrical stimulation of the motor and visual areas of the cerebral cortex in both caudate nuclei and the substantia nigra in the cat. Brain Res 145: 69–83

    Google Scholar 

  • Nieoullon A, Kerkerian L, Dusticier N (1983) Presynaptic controls in the neostriatum: Reciprocal interactions between the nigrostriatal dopaminergic neurons and the cortico-striatal glutamatergic pathway. Exp Brain Res [Suppl] 7: 54–65

    Google Scholar 

  • Péchadre JC, Larochelle L, Poirier LJ (1976) Parkinsonian akinesia, rigidity and tremor in the monkey. J Neurol Sci 28: 147–157

    Google Scholar 

  • Poirier LJ (1960) Experimental and histological study of midbrain dyskinesias. J Neurophysiol 23: 534–551

    Google Scholar 

  • Roth RH, Murrin LC, Walters JR (1976) Central dopaminergic neurons: effects of alterations in impulse flow on the accumulation of dihydroxyphenylacetic acid. Eur J Pharmacol 36: 163–171

    Google Scholar 

  • Ruffieux A, Schultz W (1980) Dopaminergic activation of reticulata neurons in the substantia nigra. Nature 285: 240–241

    Google Scholar 

  • Schultz W (1982) Depletion of dopamine in the striatum as an experimental model of Parkinsonism: direct effects and adaptive mechanisms. Progr Neurobiol 18: 121–166

    Google Scholar 

  • Schultz W, Aebischer P, Ruffieux A (1983) The encoding of motor acts by the substantia nigra. Exp Brain Res [Suppl] 7: 171–180

    Google Scholar 

  • Shanta TR, Manocha SL, Bourne GH (1968) A stereotaxic atlas of the Java Monkey brain (Macaca irus). Karger, Basel

    Google Scholar 

  • Siegel S (1956) Nonparametric statistics for the behavioral siences. Mac Graw Hill, New York

    Google Scholar 

  • Siegfried B, Bures J (1978) Asymmetry of EEG arousal in rats with unilateral 6-hydroxydopamine lesions of substantia nigra: quantification of neglect. Exp Neurol 62: 173–190

    MathSciNet  MATH  Google Scholar 

  • Steinfels GF, Heym J, Jacobs BL (1981) Single unit activity of dopaminergic neurons in freely moving cats. Life Sci 29: 1435–1442

    Google Scholar 

  • Trulson ME, Preussler DW, Howell GA (1981) Activity of substantia nigra units across the sleep-waking cycle in freely moving cats. Neurosci Lett 26: 183–188

    Google Scholar 

  • Tulloch IF, Arbuthnott GW (1979) Electrophysiological evidence for an input from the anterior olfactory nucleus to substantia nigra. Exp Neurol 66: 16–29

    Google Scholar 

  • Yamamoto BK, Freed CR (1982) The trained circling rat: a model for inducing unilateral caudate dopamine metabolism. Nature 298: 467–468

    Google Scholar 

Download references

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Supported by the Swiss National Science Foundation, grant nos. 3.446.74 and 3.752.80, and the Sandoz Foundation

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Schultz, W., Ruffieux, A. & Aebischer, P. The activity of pars compacta neurons of the monkey substantia nigra in relation to motor activation. Exp Brain Res 51, 377–387 (1983). https://doi.org/10.1007/BF00237874

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