Abstract
Cells in the inferior olive are the sole source of climbing fibers to the cerebellum. In this article, we review some of the discharge properties of olivary cells that are important for understanding its functional role in cerebellar processing. It is generally believed that climbing fiber input supplies the cerebellum with information related to movement errors in order to improve motor performance. As a whole, olivary properties are not consistent with this function. The properties are consistent with the hypothesis that the olive is important for associating arbitrary sensory stimuli with somatosensory events. Although such associations would not be useful for improving the accuracy of motor commands, they may be useful for organizing appropriate behaviors to cope with the predicted event.
Similar content being viewed by others
References
Armstrong DM. Functional significance of connections of the inferior olive. Physiol Rev 1974; 54(2): 358–417.
Armstrong DM, Campbell NC, Edgley SA, Schild RF, Trott JR. Investigations of the Olivocerebellar and Spino-Olivary Pathways. In: Palay SL, Chan-Palay V, editors. The Cerebellum — New Vistas. Berlin: Springer-Verlag, 1982.
Ito M. The Cerebellum and Neural Control. New York: Raven, 1984.
Courville J, De Montigny C, Lamarre Y. The Inferior Oliveary Nucleus: Anatomy and Physiology. New York: Raven, 1980.
Gellman R, Houk JC, Gibson AR. Somatosensory properties of the inferior olive of the cat. J Comp Neurol 1983; 215(2): 228–243.
Oscarsson O, Sjolund B. The ventral spino-olivocerebellar system in the cat. I. Identification of five paths and their termination in the cerebellar anterior lobe. Exp Brain Res 1977; 28(5): 469–486.
Oscarsson O, Sjolund B. The ventral spino-olivocerebellar system in the cat. II. Termination zones in the cerebellar posterior lobe. Exp Brain Res 1977; 28(5): 487–503.
Oscarsson O, Sjolund B. The ventral spino-olivocerebellar system in the cat. III. Functional characteristics of the five paths. Exp Brain Res 1977; 28(5): 505–520.
Eccles JC, Llinas R, Sasaki K. Intracellularly recorded responses of the cerebellar Purkinje cells. Exp Brain Res 1966; 1(2): 161–183.
Courville J, Faraco-Cantin F. On the origin of the climbing fibers of the cerebellum. An experimental study in the cat with an autoradiographic tracing method. Neuroscience 1978; 3(9): 797–809.
Groenewegen HJ, Voogd J, Freedman SL. The parasagittal zonation within the olivocerebellar projection. II. Climbing fiber distribution in the intermediate and hemispheric parts of cat cerebellum. J Comp Neurol 1979; 183(3): 551–601.
Shinoda Y, Sugihara I, Wu HS, Sugiuchi Y. The entire trajectory of single climbing and mossy fibers in the cerebellar nuclei and cortex. Prog Brain Res 2000; 124: 173–186.
Schild RF. On the inferior olive of the albino rat. J Comp Neurol 1970; 140(3): 255–260.
Eccles JC, Ito M, Szentagothai J. The Cerebellum as a Neuronal Machine. New York: Springer, 1967.
Eccles JC, Llinas R, Sasaki K. The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J Physiol 1966; 182(2): 268–296.
Jasmin L, Courville J, Bakker DA. Afferent projections from forelimb muscles to the external and main cuneate nuclei in the cat. A study with transganglionic transport of horseradish peroxidase. Anat Embryol 1985; 171(3): 275–284.
Jasmin L, Courville J. Distribution of external cuneate nucleus afférents to the cerebellum: II. Topographical distribution and zonal pattern — an experimental study with radioactive tracers in the cat. J Comp Neurol 1987; 261(4): 497–514.
Nyberg G, Blomqvist A. The central projection of muscle afferent fibres to the lower medulla and upper spinal cord: an anatomical study in the cat with the transganglionic transport method. J Comp Neurol 1984; 230(1): 99–109.
van Kan PL, Gibson AR, Houk JC. Movement-related inputs to intermediate cerebellum of the monkey. [Erratum appears in J Neurophysiol 1993 Mar;69(3)]. J Neurophysiol 1993; 69(1): 74–94.
Mackie PD, Morley JW, Rowe MJ. Signalling of static and dynamic features of muscle spindle input by external cuneate neurones in the cat. J Physiol 1999; 519 Pt 2: 559–569.
Glickstein M, May JG, 3rd, Mercier BE. Corticopontine projection in the macaque: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol 1985; 235(3): 343–359.
Glickstein M, Gerrits N, Kralj-Hans I, Mercier B, Stein J, Voogd J. Visual pontocerebellar projections in the macaque. J Comp Neurol 1994; 349(1): 51–72.
Legg CR, Mercier B, Glickstein M. Corticopontine projection in the rat: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol 1989; 286(4): 427–441.
Brodai P. The corticopontine projection from the visual cortex in the cat. II. The projection from areas 18 and 19. Brain Res 1972; 39(2): 319–335.
Brodai P. The corticopontine projection from the visual cortex in the cat. I. The total projection and the projection from area 17. Brain Res 1972; 39(2): 297–317.
Cajal SRY. Histology of the Nervous System Volume I. Translated from the French by Swanson N, Swanson LW, 1995. New York: Oxford University Press, 1909.
Baker J, Gibson A, Glickstein M, Stein J. Visual cells in the pontine nuclei of the cat. J Physiol 1976; 255(2): 415–433.
Andersson G, Armstrong DM. Complex spikes in Purkinje cells in the lateral vermis (b zone) of the cat cerebellum during locomotion. J Physiol 1987; 385: 107–134.
Harvey RJ, Porter R, Rawson JA. The natural discharges of Purkinje cells in paravermal regions of lobules V and VI of the monkey’s cerebellum. J Physiol 1977; 271(2): 515–536.
Thach WT. Discharge of cerebellar neurons related to two maintained postures and two prompt movements. II. Purkinje cell output and input. J Neurophysiol 1970; 33(4): 537–547.
Gellman R, Gibson AR, Houk JC. Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. J Neurophysiol 1985; 54(1): 40–60.
Dugas C, Smith AM. Responses of cerebellar Purkinje cells to slip of a hand-held object. J Neurophysiol 1992; 67(3): 483–495.
Horn KM, Van Kan PL, Gibson AR. Reduction of rostral dorsal accessory olive responses during reaching. J Neurophysiol 1996; 76(6): 4140–4151.
Armstrong DM, Eccles JC, Harvey RJ, Matthews PB. Responses in the dorsal accessory olive of the cat to stimulation of hind limb afferents. J Physiol 1968; 194(1): 125–145.
Crill WE. Unitary multiple-spiked responses in cat inferior olive nucleus. J Neurophysiol 1970; 33(2): 199–209.
Llinas R, Baker R, Sotelo C. Electrotonic coupling between neurons in cat inferior olive. J Neurophysiol 1974; 37(3): 560–571.
Llinas R, Yarom Y. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol 1981; 315: 549–567.
Kolb FP, Rubia FJ. Information about peripheral events conveyed to the cerebellum via the climbing fiber system in the decerebrate cat. Exp Brain Res 1980; 38(4): 363–373.
Lang EJ, Sugihara I, Welsh JP, Llinas R. Patterns of spontaneous Purkinje cell complex spike activity in the awake rat. J Neuro-science 1999; 19(7): 2728–2739.
Kitazawa S, Kimura T, Yin PB. Cerebellar complex spikes encode both destinations and errors in arm movements. Nature 1998; 392(6675): 494–497.
Fu QG, Mason CR, Flament D, Coltz JD, Ebner TJ. Movement kinematics encoded in complex spike discharge of primate cerebellar Purkinje cells. Neuroreport 1997; 8(2): 523–529.
Murphy JT, Sabah NH. Cerebellar Purkinje cell responses to afferent inputs. I. Climbing fiber activation. Brain Res 1971; 25(3): 449–467.
Robinson FR, Fraser MO, Hollerman JR, Tomko DL. Yaw direction neurons in the cat inferior olive. J Neurophysiol 1988; 60(5): 1739–1752.
Eccles JC, Sabah NH, Schmidt RF, Taborikova H. Cutaneous mechanoreceptors influencing impulse discharges in cerebellar cortex. III. In Purkinje cells by climbing fiber input. Exp Brain Res 1972; 15(5): 484–497.
Rushmer DS, Woollacott MH, Robertson LT, Laxer KD. Somatotopic organization of climbing fiber projections from low threshold cutaneous afferents to pars intermedia of cerebellar cortex in the cat. Brain Res 1980; 181(1): 17–30.
Rushmer DS, Roberts WJ, Augter GK. Climbing fiber responses of cerebellar Purkinje cells to passive movement of the cat forepaw. Brain Res 1976; 106(1): 1–20.
Spence SJ, Saint-Cyr JA. Comparative topography of projections from the mesodiencephalic junction to the inferior olive, vestibular nuclei, and upper cervical cord in the cat. J Comp Neurol 1988; 268(3): 357–374.
Berkley KJ, Hand PJ. Projections to the inferior olive of the cat. II. Comparisons of input from the gracile, cuneate and the spinal trigeminal nuclei. J Comp Neurol 1978; 180(2): 253–264.
Boesten AJ, Voogd J. Projections of the dorsal column nuclei and the spinal cord on the inferior olive in the cat. J Comp Neurol 1975; 161(2): 215–237.
Gerrits NM, Voogd J, Magras IM. Vestibular afferents of the inferior olive and the vestibulo-olivo-cerebellar climbing fiber pathway to the flocculus in the cat. Brain Res 1985; 332(2): 325–336.
Saint-Cyr JA, Courville J. Projection from the vestibular nuclei to the inferior olive in the cat: an autoradiographic and horseradish peroxidase study. Brain Res 1979; 165(2): 189–200.
de Zeeuw CI, Wylie DR, Stahl JS, Simpson JI. Phase relations of Purkinje cells in the rabbit flocculus during compensatory eye movements. J Neurophysiol 1995; 74(5): 2051–2064.
Ghelarducci B, Ito M, Yagi N. Impulse discharges from flocculus Purkinje cells of alert rabbits during visual stimulation combined with horizontal head rotation. Brain Res 1975; 87(1): 66–72.
Leonard CS, Simpson JI. Simple spike modulation of floccular Purkinje cells during the reversible blockade of their climbing fiber afferents. In: Keller EL, Zee DS, editors. Adaptive Processes in the Visual and Oculomotor Systems. Oxford, UK: Pergamon, 1986.
Precht W, Simpson JI, Llinas R. Responses of Purkinje cells in rabbit nodulus and uvula to natural vestibular and visual stimuli. Pflugers Archiv — Eur J Physiol 1976; 367(1): 1–6.
Takeda T, Maekawa K. The origin of the pretecto-olivary tract. A study using the horseradish peroxidase method. Brain Res 1976; 117(2): 319–325.
Maekawa K, Takeda T. Afferent pathways from the visual system to the cerebellar flocculus of the rabbit. In: Baker R, Berthoz A, editors. Control of Gaze by Brainstem Neurons. Amsterdam: Elsevier/ North Holland Biomed Press, 1977: 187–196.
Soodak RE, Simpson JI. The accessory optic system of rabbit. I. Basic visual response properties. J Neurophysiol 1988; 60(6): 2037–2054.
Barmack NH, Simpson JI. Effects of microlesions of dorsal cap of inferior olive of rabbits on optokinetic and vestibuloocular reflexes. J Neurophysiol 1980; 43(1): 182–206.
Barmack NH, Hess DT. Multiple-unit activity evoked in dorsal cap of inferior olive of the rabbit by visual stimulation. J Neurophysiol 1980; 43(1): 151–164.
Stone LS, Lisberger SG. Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. II. Complex spikes. J Neurophysiol 1990; 63(5): 1262–1275.
Simpson JI, Belton T, Suh M, Winkelman B. Complex spike activity in the flocculus signals more than the eye can see. Ann New York Acad Sciences 2002; 978: 232–236.
Bauswein E, Kolb FP, Leimbeck B, Rubia FJ. Simple and complex spike activity of cerebellar Purkinje cells during active and passive movements in the awake monkey. J Physiol 1983; 339: 379–394.
Mortimer JA. Cerebellar responses to teleceptive stimuli in alert monkeys. Brain Res 1975; 83(3): 369–390.
Matthews PBC. Mammalian Muscle Receptors and Their Central Actions. London: Edward Arnold, 1972.
Jasmin L, Courville J. Distribution of external cuneate nucleus afferents to the cerebellum: I. Notes on the projections from the main cuneate and other adjacent nuclei. An experimental study with radioactive tracers in the cat. J Comp Neurol 1987; 261(4): 481–496.
Matsushita M, Ikeda M. Spinocerebellar projections from the cervical enlargement in the cat, as studied by anterograde transport of wheat germ agglutinin-horseradish peroxidase. J Comp Neurol 1987; 263(2): 223–240.
McCurdy ML, Houk JC, Gibson AR. Organization of ascending pathways to the forelimb area of the dorsal accessory olive in the cat. J Comp Neurol 1998; 392(1): 115–133.
Ekerot CF, Gustavsson P, Oscarsson O, Schouenborg J. Climbing fibres projecting to cat cerebellar anterior lobe activated by cutaneous A and C fibres. J Physiol 1987; 386: 529–538.
Ekerot CF, Oscarsson O, Schouenborg J. Stimulation of cat cutaneous nociceptive C fibres causing tonic and synchronous activity in climbing fibres. J Physiol 1987; 86: 539–546.
Garwicz M, Ekerot CF, Schouenborg J. Distribution of cutaneous nociceptive and tactile climbing fibre input to sagittal zones in cat cerebellar anterior lobe. Eur J Neurosci 1992; 4(4): 289–295.
Rawson JA, Tilokskulchai K. Climbing fibre modification of cerebellar Purkinje cell responses to parallel fibre inputs. Brain Res 1982; 237(2): 492–497.
Ekerot CF. Climbing fibres — a key to cerebellar function. J Physiol 1999; 516(Pt 3): 629.
Rubia FJ. The projection of visceral afferents to the cerebellar cortex of the cat. Pflugers Archiv — Eur J Physiol 1970; 320(2): 97–110.
Tong G, Robertson LT, Brons J. Vagal and somatic representation by the climbing fiber system in lobule V of the cat cerebellum. Brain Res 1991; 552(1): 58–66.
Tong G, Robertson LT, Brons J. Climbing fiber representation of the renal afferent nerve in the vermal cortex of the cat cerebellum. Brain Res 1993; 601(1–2): 65–75.
Hennemann HE, Rubia FJ. Vagal representation in the cerebellum of the cat. Pflugers Archiv -Eur J Physiol 1978; 375(2): 119–123.
Perrin J, Crousillat J. Responses of single units in the inferior olive nucleus to stimulation of the splanchnic afferents in the cat. J Auton Nerv Syst 1980; 2(1): 15–22.
Nishii K, Oura C, Pallie W. Ultrastructure of the mature Pacinian corpuscle in the mesentery of the cat. J Anat 1970; 106(1): 208.
Garwicz M, Ekerot CF. Topographical organization of the cerebellar cortical projection to nucleus interpositus anterior in the cat. J Physiol 1994; 474(2): 245–260.
Martin RJ, Apkarian AV, Hodge CJ, Jr. Ventrolateral and dorsolateral ascending spinal cord pathway influence on thalamic nociception in cat. J Neurophysiol 1990; 64(5): 1400–1412.
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 1988; 400: 405–414.
Apps R. Movement-related gating of climbing fibre input to cerebellar cortical zones. Prog Neurobiol 1999; 57(5): 537–562.
Nelson BJ, Adams JC, Barmack NH, Mugnaini E. Comparative study of glutamate decarboxylase immunoreactive boutons in the mammalian inferior olive. J Comp Neurol 1989; 286(4): 514–539.
de Zeeuw CI, Holstege JC, Calkoen F, Ruigrok TJ, 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(2): 369–375.
Angaut P, Sotelo C. The dentato-olivary projection in the rat as a presumptive GABAergic link in the olivo-cerebello-olivary loop. An ultrastructural study. Neurosci Lett 1987; 83(3): 227–231.
Angaut P, Sotelo C. Synaptology of the cerebello-olivary pathway. Double labelling with anterograde axonal tracing and GABA immunocytochemistry in the rat. Brain Res 1989; 479(2): 361–365.
Gibson AR, Horn KM, Pong M. Inhibitory control of olivary discharge. In: Highstein SM, Thach WT, editors. The Cerebellum: Recent Developments in Cerebellar Research, Ann New York Acad Sciencesvol. 9782002.
Oscarsson O. Functional organization of olivary projection to the cerebellar anterior lobe. In: Courville J, De Montigny C, Lamarre Y, editors. The Inferior Olivary Nucleus: Anatomy and Physiology. New York: Raven Press, 1980: 279–289.
Horn KM, Pong M, Gibson A. Discharge of inferior olive cells during reaching errors and perturbations. Brain Res 2004; 996(2): 148–158.
Gibson AR, Robinson FR, Alam J, Houk JC. Somatotopic alignment between climbing fiber input and nuclear output of the cat intermediate cerebellum. J Comp Neurol 1987; 260(3): 362–377.
Gellman R, Miles F. A new role for the cerebellum in condizioning? Trends Neurosci 1985; 8(1): 181–182.
Yeo CH, Hardiman MJ, Glickstein M. Classical conditioning of the nictitating membrane response of the rabbit. IV. Lesions of the inferior olive. Exp Brain Res 1986; 63(1): 81–92.
Welsh JP, Harvey JA. Acute inactivation of the inferior olive blocks associative learning. Eur J Neurosci 1998; 10(11): 3321–3332.
McCormick DA, Steinmetz JE, Thompson RF. Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Res 1985; 359(1–2): 120–130.
Medina JF, Nores WL, Mauk MD. Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 2002; 416(6878): 330–333.
Voneida TJ, Christie D, Bogdanski R, Chopko B. Changes in instrumentally and classically conditioned limb-flexion responses following inferior olivary lesions and olivocerebellar tractotomy in the cat. J Neurosci 1990; 10(11): 3583–3593.
Pavlov. Conditioned Reflexes. London, England: Oxford University Press, 1927.
Bower JM. The organization of cerebellar cortical circuitry revisited: implications for function. Ann New York Acad Sciences 2002; 978: 135–155.
Bloedel JR, Roberts WJ. Action of climbing fibers in cerebellar cortex of the cat. J Neurophysiol 1971; 34(1): 17–31.
Gibson AR, Gellman R. Functional implications of inferior olivary response properties. In: Glickstein M, Yeo C, Stein J, editors. Cerebellum and Neuronal Plasticity: Plenum, 1987: 119–140.
Hausser M, Major G, Stuart GJ. Differential shunting of EPSPs by action potentials. Science 2001; 291(5501): 138–141.
Jorntell H, Ekerot CF. Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 2002; 34(5): 797–806.
Bull MS, Berkley KJ. Differences in the neurons that project from the dorsal column nuclei to the diencephalon, pretectum, and tectum in the cat. Somatosens Res 1984; 1(3): 281–300.
Bull MS, Mitchell SK, Berkley KJ. Convergent inputs to the inferior olive from the dorsal column nuclei and pretectum in the cat. Brain Res 1990; 525(1): 1–10.
Berkley KJ, Worden IG. [Projections to the inferior olive of the cat. I. Comparisons of input from the dorsal column nuclei, the lateral cervical nucleus, the spino-olivary pathways, the cerebral cortex and the cerebellum.]. J Comp Neurol 1978; 180(2): 237–251.
Maekawa K, Simpson JL. Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system. J Neurophysiol 1973; 36(4): 649–666.
Kyuhou S, Matsuzaki R. Topographical organization of the tectoolivo-cerebellar projection in the cat. Neuroscience 1991; 41(1): 227–241.
Onodera S. Olivary projections from the mesodiencephalic structures in the cat studied by means of axonal transport of horseradish peroxidase and tritiated amino acids. J Comp Neurol 1984; 227(1): 37–49.
Loewy AD, Burton H. Nuclei of the solitary tract: efferent projections to the lower brain stem and spinal cord of the cat. J Comp Neurol 1978; 181(2): 421–449.
Huerta MF, Hashikawa T, Gayoso MJ, Harting JK. The trigemino-olivary projection in the cat: contributions of individual subnuclei. J Comp Neurol 1985; 241(2): 180–190.
Akaike T. Spatial distribution of evoked potentials in the inferior olivary nucleus by stimulation of the visual afferents in the rat. Brain Res 1986; 368(1): 183–187.
Barmack NH, Fredette BJ, Mugnaini E. Parasolitary nucleus: a source of GABAergic vestibular information to the inferior olive of rat and rabbit. J Comp Neurol 1998; 392(3): 352–372.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gibson, A.R., Horn, K.M. & Pong, M. Activation of climbing fibers. Cerebellum 3, 212–221 (2004). https://doi.org/10.1080/14734220410018995
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1080/14734220410018995