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The great gate: Control of sensory information flow to the cerebellum

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Abstract

An evident feature of the physiology of the inferior olivary nucleus is modulation of the responsiveness of neurons to peripheral stimulation by the behavioral state of the subject animal. The olivary response to self-generated sensory inputs, as well as to input predictable from association with other stimuli, is suppressed. This suppression occurs in part at the level of the inferior olivary nucleus itself. On the other hand, the cells respond readily to sensory inputs that are not anticipated. On a cellular level inferior olivary neurons exhibit two properties that might account for information gating. The first one is the organization of synaptic inputs on olivary spines in glomerular structures, where extrinsic inhibitory and excitatory inputs, confined to the same olivary dendritic spine, can efficiently cancel each other if they arrive within a certain time window. About half of the inhibitory inputs to olivary glomeruli originate in the deep cerebellar nuclei and are regarded as an inhibitory feedback. The second property is subthreshold membrane potential oscillations, a property of the electrotonically coupled olivary network. Extrinsic synaptic inputs to the nucleus modulate the subthreshold oscillations, and consequently, the response properties of olivary neurons. A considerable amount of indirect evidence indicates that the occurrence of oscillations corresponds to states of increased responsiveness of the neurons to peripheral stimulation. The sensory filtering role of the inferior olivary nucleus invites comparison between the cerebellum and cerebellar-like structures. This comparison sheds important light on the function of the cerebellum.

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References

  1. Oscarsson O. Functional organization of olivary projection to the cerebellar anterior lobe. In: Courville JC, de Montigny C, Lamarre Y, editors. The inferior olivary nucleus. New York: Raven Press, 1980: 279–289.

    Google Scholar 

  2. DuLac S, Raymond JL, Sejnowski TJ, Lisberger SG. Learning and memory in the vestibulo-ocular reflex. Annu Rev Neurosci 1995; 18: 409–441.

    Article  CAS  Google Scholar 

  3. Snider RS. A tectocerebellar pathway. Anat Rec 1945; 91: 299.

    Google Scholar 

  4. Schmahmann JD, Pandya DN. The cerebrocerebellar system. In: Schmahmann JD, editor. The cerebellum and cognition. San Diego: Academic Press; 1997: 31–60.

    Google Scholar 

  5. Coltz JD, Johnson MTV, Ebner TJ. Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking. J Neurosci 1999; 19: 1782–1803.

    PubMed  CAS  Google Scholar 

  6. Perciavalle V, Bosco G, Poppele R. Correlated activity in the spinocerebellum is related to spinal timing generators. Brain Res 1995; 695: 293–297.

    PubMed  CAS  Google Scholar 

  7. Bower JM, Woolston DC. Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. J Neurophysiol 1983; 49: 745–765.

    PubMed  CAS  Google Scholar 

  8. Armstrong DM, Edgley SA. Discharges of Purkinje cells in the paravermal part of the cerebellar anterior lobe during locomotion in the cat. J Physiol (Lond) 1984; 352: 403–424.

    CAS  Google Scholar 

  9. Barmack NH, Shojaku H. Vestibular and visual climbing fiber signals evoked in the uvula-nodulus of the rabbit cerebellum by natural stimulation. J Neurophysiol 1995; 74: 2573–2589.

    PubMed  CAS  Google Scholar 

  10. Gellman RS, Houk JC, Gibson AR. Somatosensory properties of the inferior olive of the cat. J Comp Neurol 1983; 215: 228–243.

    Article  PubMed  CAS  Google Scholar 

  11. Garwicz M, Jorntell H, Ekerot C-F. Cutaneous receptive fields and topography of mossy fibers and climbing fibers projecting to cat cerebellar C3 zone. J Physiol (Lond) 1998; 512: 277–293.

    Article  CAS  Google Scholar 

  12. Gellman RS, Gibson AR, Houk JC. Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. J Neurophysiol 1985; 54: 40–60.

    PubMed  CAS  Google Scholar 

  13. Ekerot C-F, Gustavsson P, Schouenborg J. Climbing fibers projecting to cat cerebellar anterior lobe activated by cutaneous A and C fibers. J Physiol (Lond) 1987; 386: 529–538.

    CAS  Google Scholar 

  14. Robertson LT. Somatosensory representation of the climbing fiber system in the rostral intermediate cerebellum. Exp Brain Res 1985; 61: 73–86.

    Article  PubMed  CAS  Google Scholar 

  15. Callaway JC, Lasser-Ross N, Ross WN. IPSPs strongly inhibit climbing fiber-activated [Ca2+]i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 1995; 15: 2777–2787.

    PubMed  CAS  Google Scholar 

  16. Ito M. Long-term depression. Annu Rev Neurosci 1989; 12: 85–102.

    Article  PubMed  CAS  Google Scholar 

  17. Kim JJ, Krupa DJ, Thompson RF. Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science 1998; 279: 570–573.

    Article  PubMed  CAS  Google Scholar 

  18. Armstrong DM, Edgley SA, Lidierth M. Complex spikes in Purkinje cells of the paravermal part of the anterior lobe of the cat cerebellum during locomotion. J Physiol (Lond) 1988; 400: 405–414.

    CAS  Google Scholar 

  19. Apps R. Movement-related gating of climbing fibre input to cerebellar cortical zones. Prog Neurobiol 1999; 57: 573–562.

    Article  Google Scholar 

  20. Baker S, Seers C, Sears TA. Respiratory modulation of afferent transmission to the cerebellum. In: Speck F, Dekin MS, Revelette WR, Fraizier DT, editors. Respiratory control. Central and peripheral mechanisms. Kentucky: University Press of Kentucky, 1993: 95–99.

    Google Scholar 

  21. Simpson JI, Wylie DR, DeZeeuw CI. On climbing fiber signals and their consequence(s). Behav Brain Sci 1996; 19: 384–398.

    Google Scholar 

  22. Thompson RF, Bao S, Chen L, Cipriano BJ, Grethe JS, Kim JJ, Thompson JK, Tracy JA, Weninger MS, Krupa DJ. Associative learning. In: Schmahmann JD, editor. The cerebellum and cognition. San Diego: Academic Press, 1997: 152–189.

    Google Scholar 

  23. Maekawa K, Simpson JI. Climbing fiber responses evoked in the vestibulocerebellum of rabbit from visual system. J Neurophysiol 1973; 36: 649–666.

    PubMed  CAS  Google Scholar 

  24. Raymond JL, Lisberger SG. Neural learning rules for vestibuloocular reflex. J Neurosci 1998; 18: 9112–9129.

    PubMed  CAS  Google Scholar 

  25. Stone LS, Lisberger SG. Visual responses of Purkinje cells in the cerebellar floculus during smooth-pursuit eye movements in monkeys II. Complex spikes. J Neurophysiol 1990; 63: 1262–1275.

    CAS  Google Scholar 

  26. Belton T, McCrea RA. Contribution of the cerebellar flocculus to gaze control during active head movements. J Neurophysiol 1999; 81: 3105–3109.

    PubMed  CAS  Google Scholar 

  27. Blakemore S-J, Wolpert DM, Frith CD. Central cancellation of self-produced tickle sensation. Nature Neurosci 1998; 1: 635–640.

    Article  PubMed  CAS  Google Scholar 

  28. Blakemore S-J, Wolpert DM, Frith CD. The cerebellum contributes to somatosensory cortical activity during self-produced tactile stimulation. NeuroImage 1999; 10: 448–459.

    Article  PubMed  CAS  Google Scholar 

  29. Ploghaus A, Tracey I, Gati JS, Clare S, Menon RS, Matthews PM, Rawlins JNP. Dissociating pain from its anticipation in the human brain. Science 1999; 284: 1979–1981.

    Article  PubMed  CAS  Google Scholar 

  30. Ploghaus A, Tracey I, Clare S, Gati JS, Menon RS, Rawlins JNP, Matthews PM. Learning about pain: the neural substrate of the prediction error for aversive events. PNAS 2000; 97: 9281–9286.

    Article  PubMed  CAS  Google Scholar 

  31. Brown IE, Bower JM. Correlations between S1 field potentials and cerebellar complex spikes in response to peripheral, tactile stimuli. Soc Neurosci Abstr 2000; 26: 1985.

    Google Scholar 

  32. Jenkinson EW, Glickstein M. Whiskers, barrels, and cortical efferent pathways in gap crossing by rats. J Neurophysiol 2000; 84: 1781–1789.

    PubMed  CAS  Google Scholar 

  33. Chapman CE. Active versus passive touch: factors influencing the transmission of somatosensory signals to primary somatosensory cortex. Can J Physiol Pharmacol 1994; 72: 558–570.

    PubMed  CAS  Google Scholar 

  34. Prochazka A. Sensorimotor gain control: a basic strategy of motor systems? Prog Neurobiol 1989; 33: 281–307.

    Article  PubMed  CAS  Google Scholar 

  35. De Zeeuw CI, Holstage JC, Ruigrok TJH, Voogd J. Ultrastructural study of the GABAergic, cerebellar, and mesodiencephalic innervation of the cat medial accessory olive: anterograde tracing combined with immunocytochemistry. J Comp Neurol 1989; 284: 12–35.

    Article  PubMed  Google Scholar 

  36. De Zeeuw CI, Ruigrok TJH, Holstege JC, Jansen HG, Voogd J. Intracellular labeling of neurons in the medial accessory olive of the cat: II. Ultrastructure of the dendritic spines and their GABAergic innervation. J Comp Neurol 1990; 300: 478–494.

    Google Scholar 

  37. De Zeeuw CI, Holstege JC, Ruigrok TJH, Voogd J. Mesodien-cephalic and cerebellar terminals terminate upon the same dendritic spines in the glomeruli of the cat and rat inferior olive: an ultrastructural study using a combination of [3H]leucine and wheat germ agglutinin coupled horseradish peroxidase anterograde tracing. Neuroscience 1990; 34: 645–655.

    Article  PubMed  Google Scholar 

  38. De Zeeuw CI, Holstege JC, Calkoen F, Ruigrok TJH, Voogd J. A new combination of WGA-HRP anterograde tracing and GABA-immunocytochemistry applied to afferents of the cat inferior olive at the ultrastructural level. Brain Res 1988; 447: 369–375.

    Article  PubMed  Google Scholar 

  39. Nelson BJ, Mugnaini E. Origins of GABAergic inputs to the inferior olive. In: Strata P, editor. The olivocerebellar system in motor control. New York: Springer-Verlag, 1989: 86–107.

    Google Scholar 

  40. Kennedy PR, Gibson AR, Houk JC. Functional and anatomic differentiation between parvicellular and magnocellular regions of red nucleus in the monkey. Brain Res 1986; 364: 124–136.

    Article  PubMed  CAS  Google Scholar 

  41. Horn KM, Hamm TM, Gibson AR. Red nucleus stimulation inhibits within the inferior olive. J Neurophysiol 1998; 80: 3127–3136.

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  43. Llinas R, Yarom Y. Electrophysiology of mammalian inferior olivary neurons in vitro. Different types of voltage-dependent ionic conductances. J Physiol (Lond) 1981; 315: 549–567.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  45. Manor Y, Yarom Y, Chorev E, Devor A. To beat or not to beat: a decision taken at the network level. J Physiol (Paris) 2000; 94: 375–390.

    Article  CAS  Google Scholar 

  46. Lampl I, Yarom Y. Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device. J. Neurophysiol 1993; 70: 2181–2186.

    PubMed  CAS  Google Scholar 

  47. Llinas R. Eighteenth Bowdwich lecture. Motor aspects of cerebellar control. Physiologist 1974; 17: 19–46.

    PubMed  CAS  Google Scholar 

  48. Devor A, Fritschy J-M, Yarom Y. Spatial distribution and subunit composition of GABAA receptors in the inferior olivary nucleus. J Neurophysiol 2001; 85: 1686–1696.

    PubMed  CAS  Google Scholar 

  49. Placantonakis DG, Schwarz C, Welsh JP. Serotonin suppresses subthreshold and suprathreshold oscillatory activity of rat inferior olivary neurones in vitro. J Physiol (Lond) 2000; 524: 833–851.

    Article  CAS  Google Scholar 

  50. Lang E. Organization of olivocerebellar activity in the absence of excitatory glutamatergic input. J Neurosci 2001; 21: 1663–1675.

    PubMed  CAS  Google Scholar 

  51. Veasey SD, Fornal CA, Metzler CW, Jacobs BL. Response to serotonergic caudal raphe neurons in relation to specific motor activities in freely moving cats. J Neurosci 1995; 15: 5346–5359.

    PubMed  CAS  Google Scholar 

  52. Keating JG, Thach WT. Nonclock behavior of inferior olive neurons: interspike interval of Purkinje cell complex spike discharge in the awake behaving monkey is random. J Neurophysiol 1995; 73: 1329–1340.

    PubMed  CAS  Google Scholar 

  53. Hartmann MJ, Bower JM. Oscillatory activity in the cerebellar hemispheres of unrestrained rats. J Neurophysiol 1998; 80: 1598–1604.

    PubMed  CAS  Google Scholar 

  54. Lang EJ, Sugihara I, Welsh JP, Llinas R. Patterns of spontaneous Purkinje cell complex spike activity in the awake rat. J Neurosci 1999; 19: 2728–2739.

    PubMed  CAS  Google Scholar 

  55. Kistler WM, van Hemmen JL, De Zeeuw CI. Time window control: a model for cerebellar function based on synchronization, reverberation, and time slicing. Prog Brain Res 2000; 124: 275–297.

    Article  PubMed  CAS  Google Scholar 

  56. Devor A. Is the cerebellum like cerebellar-like structures? Brain Res Rev 2000; 34: 149–156.

    Article  PubMed  CAS  Google Scholar 

  57. Brown IE, Bower JM. Congruence of mossy fiber and climbing fiber tactile projections in the lateral hemispheres of the rat cerebellum. J Comp Neurol 2001; 429: 57–70.

    Article  Google Scholar 

  58. Ekerot C-F, Jorntell H. Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific. Eur J Neurosci 2001; 13: 1303–1310.

    Article  PubMed  CAS  Google Scholar 

  59. Thompson RF. Role of inferior olive in classical conditioning. In: Strata P, editor. The olivocerebellar system in motor control. New York: Springer-Verlag, 1989: 347–362.

    Google Scholar 

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Correspondence to Anna Devor.

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Devor, A. The great gate: Control of sensory information flow to the cerebellum. Cerebellum 1, 27–34 (2002). https://doi.org/10.1080/147342202753203069

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