Skip to main content

Parkinsonian Tremor is Associated with Low Frequency Neuronal Oscillations in Selective Loops of the Basal Ganglia

  • Chapter
The Basal Ganglia IV

Part of the book series: Advances in Behavioral Biology ((ABBI,volume 41))

Abstract

Parkinsonian tremor (Lance et al., 1963; Findley et al., 1981; Elble and Koller, 1990), has most often been attributed to neuronal oscillatory activity in cerebello-thalamocortical, rather than in basal ganglia-thalamocortical circuits. This notion is supported by several lines of evidence. Lesions of the substantia nigra produce tremor in monkeys only in combination with damage to cerebellorubral, and cerebellothalamic pathways (Poirier, 1960). Similarly, systemic treatment of monkeys with the neurotoxin l-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP), which causes clinical and pathological changes closely resembling human parkinsonism (e.g., DeLong, 1990), does not result in low frequency tremor in most primate species (Burns et al., 1983; Langston et al., 1984; Jenner et al., 1986). In addition, periodic oscillatory neuronal activity was found in the cerebello-thalamocortical circuits in animal models of tremor in in-vitro (Llinas and Yarom, 1981a,b; Jahnsen and Llinas, 1984a,b) and in-vivo studies (de Montigny and Lamarre, 1973; Llinas and Volkind, 1973; Lamarre and Joffroy, 1979). Furthermore, parkinsonian tremor in humans is effectively reduced by thalamic lesions, especially when placed in the Vim nucleus, the cerebellar receiving area of the ventrolateral thalamus. In fact, electrophysiological recording during lesioning surgeries revealed rhythmic neuronal discharge in Vim, in synchrony with tremor (Ohye et al., 1974; Lenz et al., 1988; Narabayashi, 1990).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Albin, R.L., Young, A.B., and Penney, J.B., 1989, The functional anatomy of basal ganglia disorders,TINS 12:366–375.

    PubMed  CAS  Google Scholar 

  • Alexander, G.E., Crutcher, M.D., and DeLong, M.R., 1990, Basal ganglia-thalamocortical circuits:parallel substrates for motor, oculomotor, ′prefrontal’ and ′limbic’ functions,Prog. Brain Res. 85:119–146.

    Article  PubMed  CAS  Google Scholar 

  • Aziz, T.Z, Peggs, D., Sambrook, M.A., and Crossman, A.R., 1991, Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism in the primates,Movement disorders 6:288–293.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bergman, H., Karmon, B., Wichmann, T., DeLong, M.R., 1993, The primate subthalamic nucleus: II. Neural activity in the subthalamic nucleus and pallidum in the MPTP model of parkinsonism,J. Neurophysiology submitted

    Google Scholar 

  • Bernheimer, H., Birkmayer, W., Hornykiewicz, O., Jellinger, K., and Seiteiberger, F., 1974, Brain dopamine and the syndromes of Parkinson and Huntington,J. Neurol. Sci 20:415–455.

    Article  Google Scholar 

  • Burns, R.S., Chiueh, CC, Markey, S.P., Ebert, M.H., Jacobowitz, D.M., and Kopin, J.J., 1983, A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine,Proc. Natl. Acad. Sci. USA 80:4546–4550.

    Article  PubMed  CAS  Google Scholar 

  • Contreras, CM., Mexicano, G., and Guzman-Flores, C, 1981, A stereotaxic brain atlas of the green monkey (Cercopithecus Aethiops Aethiops),Bol. Est. Med. Biol., Mex. 31:383–428.

    CAS  Google Scholar 

  • DeLong, M.R., Crutcher, M.D., and Georgopoulos, A.P., 1985, Primate globus pallidus and subthalamic nucleus: Functional organization,J. Neurophysiol. 53:530–543.

    PubMed  CAS  Google Scholar 

  • DeLong, M.R., 1990, Primate models of movement disorder of basal ganglia origin,TINS 13:281–285.

    PubMed  CAS  Google Scholar 

  • de Montigny, C, and Lamarre, Y., 1973, Rhythmic activity induced by harmaline in the olivo-cerebello-bulbar system of the cat,Brain Res. 53:81–95.

    Article  PubMed  Google Scholar 

  • Deschênes, M., Paradis, M., Roy, J.P., and Steriade, N., 1984, Electrophysiology of neurons of lateral thalamic nuclei in cat:resting properties and burst discharge,J. Neurophysiology 51:1196–1219.

    Google Scholar 

  • Elble, R.J., Koller, W.C., 1990, “Tremor,” The John Hopkins University Press, Baltimore and London.

    Google Scholar 

  • Elsworth, J.D., Deutch, A.Y., Redmond, D.E., Sladek, J.R., and Roth, R.H., 1987, Differential responsiveness to 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine toxicity in subregions of the primate substantia nigra and striatum,Life Sciences 40:193–202.

    Article  PubMed  CAS  Google Scholar 

  • Filion, M., 1979, Effects of interruption of the nigrostriatal pathway and dopaminergic agents on the spontaneous activity of globus pallidus neurons in a awake monkey,Brain Res. 178:425–441.

    Article  PubMed  CAS  Google Scholar 

  • Filion, M., Tremblay, L., and Bédard, P.J., 1988, Abnormal influences of passive limb movement on the activity of globus pallidus neurons in parkinsonian monkeys,Brain Res. 444:165–176.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Findley, L.J., Gresty, M.A., and Halmagyi, G.M., 1981, Tremor, the cogwheel phenomena and clonus in Parkinson’s disease,J. Neurol. Neurosurg. Psychiatry 44:534–546.

    Article  PubMed  CAS  Google Scholar 

  • Glass, L., Mackey, M.C., 1988, “From Clocks to Chaos,” Princeton University Press, N.J.

    Google Scholar 

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

    Google Scholar 

  • Jahnsen, H., and Llinas, R., 1984a, Electrophysiological properties of guinea-pig thalamic neurones:an in vitro study,J. Physiol. 349:205–226.

    CAS  Google Scholar 

  • Jahnsen, H., and Llinas, R., 1984b, Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro,J. Physiol. 349:227–247.

    CAS  Google Scholar 

  • Jenner, P., Rose, S., Nomto, M, Marsden, CD., 1986, MPTP-induced parkinsonism in the common marmoset: behavioral and biochemical effectsin: “Advances in Neurology, Vol 45,” M.F. Yahr, K.J. Bergmann, eds., Raven Press, New York, pp. 183–190.

    Google Scholar 

  • Karmon, B., Bergman, H., 1993, Detection of neuronal periodic oscillations in the basal ganglia of normal and parkinsonian monkeys,Is. J. Med. Sci. submitted.

    Google Scholar 

  • Kita, H., 1992, Responses of globus pallidus neurons to cortical stimulation:intracellular study in rat,Brain Res. 589:84–90.

    Article  PubMed  CAS  Google Scholar 

  • Laitinen, L.V., Bergenheim, A.T., and Hariz, M.I., 1992, Leksell’s posteroventral pallidotomy in the treatment of Parkinson disease,J. Neurosurg. 76:53–61.

    Article  PubMed  CAS  Google Scholar 

  • Lamarre, Y., and Joffroy, A.J., 1979, Experimental tremor in monkey:Activity of thalamic and precentrai cortical neurons in the absence of peripheral feedback, in:“Advances in Neurology, Vol. 24,” L.J. Poirier, T.L. Sourkes and P.J. Bédard, eds, Raven Press, New York, pp. 109–122.

    Google Scholar 

  • Lance, J.W., Schwab, R.S., and Peterson, E.A., 1963, Action tremor and the cogwheel phenomena in Parkinson’s disease,Brain 86:95–110.

    Article  PubMed  CAS  Google Scholar 

  • Langston, J.W., Forno, L.S., Rebert, C.S., and Irwin, I., 1984, Selective nigral toxicity after systemic administration of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine (MPTP) in the squirrel monkey,Brain Res. 292:390–394.

    Article  PubMed  CAS  Google Scholar 

  • Lavoie, B., Smith, Y., and Parent, A., 1989, Dopaminergic innervation of the basal ganglia in the squirrel monkey as revealed by tyrosine hydroxylase immunohistochemistry,J. Comp. Neurol. 289:36–52.

    Article  PubMed  CAS  Google Scholar 

  • Lenz, FA., Tasker, R.R., Kwan, H.C., Schider, S., Kwong, R., Dorsrovsky, J.O., and Murphy, J.T., 1988, Single unit analysis of the human ventral thalamic nuclear group:correlation of thalamic “tremor cells” with the 3–6 Hz component of parkinsonian tremor,J. Neurosci. 8:754–764.

    PubMed  CAS  Google Scholar 

  • Llinas, R.R., 1988, The intrinsic electrophysiological properties of mammalian neurons:Insights into central nervous system function,Science 242:1654–1664.

    Article  PubMed  CAS  Google Scholar 

  • Llinas, R.R., and Volkind, R.A., 1973, The olivo-cerebello system:functional properties as revealed by harmaline induced tremor,Exp. Brain Res. 18:69–87.

    Article  PubMed  CAS  Google Scholar 

  • Llinas, R.R., and Yarom, Y., 1981a, Electrophysiology of mammalian inferior olivary neurons in vitro. Different types of voltage dependent ionic conductance,J. Physiol. 315:549–567.

    PubMed  CAS  Google Scholar 

  • Llinas, R.R., and Yarom, Y., 1981b, Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurons in vitro,J. Physiol. 315:569–584.

    PubMed  CAS  Google Scholar 

  • Llinas, R.R., and Yarom, Y., 1986, Oscillatory properties of guinea-pig inferior olivary neurons and their pharmacological modulation:an in vitro study,J. Physiol. 376:163–182.

    PubMed  CAS  Google Scholar 

  • Llinas, R.R., Grace, A.A., and Yarom, Y., 1991, In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50 Hz frequency range,Proc. Natl. Acad. Sci. USA 88:897–901.

    Article  PubMed  CAS  Google Scholar 

  • Miller, W.C., 1988, “Examination of the motor abnormalities and changes in neuronal activity in the globus pallidus in the primate MPTP model of parkinsonism,” Ph.D. thesis, Baltimore

    Google Scholar 

  • Miller, W.C., DeLong, M.R., 1987, Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism, in: “The Basal Ganglia II,” M.B. Carpenter, A. Jayaraman, eds., Plenum Press, New York, pp. 415–427.

    Google Scholar 

  • Nakanishi, H., Hori N., and Katsuda, N., 1985, Neostriatal evoked inhibition and the effects of dopamine on globus pallidus neurons in rat slice preparations,Brain Res. 358:282–286.

    Article  PubMed  CAS  Google Scholar 

  • Nambu, A., and Llinas, R.R., 1990, Electrophysiology of the globus pallidus neurons:an in vitro study in guinea pig brain slices,Soc. Neurosci. Abstr. 16:428.

    Google Scholar 

  • Narabayashi, H., 1990, Surgical Treatment in the Levodopa era,in: “Parkinson’s disease,” G. Stern, ed.,Chapamn & Hall, London, pp. 597–646

    Google Scholar 

  • Ohye, C, Saito, U., and Fukamachi, A., 1974, An analysis of the spontaneous rhythmic and non–rhythmic burst discharge in the human thalamic,J. Neurol. Sci. 22:245–259.

    Article  PubMed  CAS  Google Scholar 

  • Paré, D., Curro’Dossi, R., and Steriade, M., 1990, Neuronal basis of the parkinsonian resting tremor:A hypothesis and its implications for treatment,Neuroscience 35:217–226.

    Article  PubMed  Google Scholar 

  • Parent, A., and Smith, Y., 1987, Differential dopaminergic innervation of the two pallidal segments in the squirrel monkey (Saimiri sciureus),Brain Res. 426:397–400.

    Article  PubMed  CAS  Google Scholar 

  • Parent, A., Lavoie, B., Smith, Y., and Bédard, P., 1990, The dopaminergic nigropallidal projection in primates:Distinct cellular origin and relative sparing in MPTP treated monkeys, in:“Advances in Neurology, Vol 53,” M.B. Streifler, A.D. Korczyn, E. Melamed and M.B.H. Youdim, eds., Raven Press, New York, pp. 111–116.

    Google Scholar 

  • Poirier, L.J., 1960, Experimental and histological study of midbrain dyskinesia,J. Neurophysiol. 23:534–551.

    PubMed  CAS  Google Scholar 

  • Redmond, D.E., Roth, R.H., and Sladek, J.R., 1985, MPTP produces classic parkinsonian syndrome in African green monkeys,Soc. Neurosci. Abstr 11:166.

    Google Scholar 

  • Schneider, J.S., and Dacko, S., 1991, Relative sparing of the dopaminergic innervation of the globus pallidus in monkeys made hemi-parkinsonian by intracarotid MPTP infusion,Brain Res. 556:292–296.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Silva, L.R., Amitai, Y., and Connors, B.W., 1991, Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons,Science 251:432–435.

    Article  PubMed  CAS  Google Scholar 

  • Svennilson, E., Torvik, A., Lowe, R., and Leksell, L., 1960, Treatment of parkinsonism by stereotactic thermolesions in the pallidal region. A clinical evaluation of 81 cases,Acta Psychiat. Neurol. Scand. 35:358–377.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wichmann, T., Bergman, H., DeLong, M.R., 1993a, The primate subthalamic nucleus I. Functional properties in intact animals,J. Neurophysiology. submitted.

    Google Scholar 

  • Wichmann, T., Bergman H., DeLong, M.R., 1993b, The primate subthalamic nucleus III. Changes in behavior and pallidal neuronal activities induced by subthalamic inactivation in the model of parkinsonism,J. Neurophysiology submitted.

    Google Scholar 

  • Winters, W.D., Kado, R.T., Adey, W.R., 1969, “A Stereotaxic Brain Atlas for Macaca nemestrina,” Univ of California Press, Berkeley and Los Angeles.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1994 Plenum Press, New York

About this chapter

Cite this chapter

Bergman, H., Wichmann, T., Karmon, B., DeLong, M.R. (1994). Parkinsonian Tremor is Associated with Low Frequency Neuronal Oscillations in Selective Loops of the Basal Ganglia. In: Percheron, G., McKenzie, J.S., Féger, J. (eds) The Basal Ganglia IV. Advances in Behavioral Biology, vol 41. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0485-2_33

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-0485-2_33

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-7591-6

  • Online ISBN: 978-1-4613-0485-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics