Skip to main content
SpringerLink
Log in

The function of the cerebellar uvula in monkey during optokinetic and pursuit eye movements: single-unit responses and lesion effects

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The cerebellum is known to participate in visually guided eye movements. The cerebellar uvula receives projections from pontine nuclei that have been implicated in visual motion processing and the generation of smooth pursuit. Single-unit and lesion studies were conducted to determine how the uvula might further process these input signals. Purkinje cells and input fibers were recorded during a variety of visual and oculomotor paradigms. Most Purkinje cells were modulated in either an excitatory or inhibitory fashion by prolonged, horizontal optokinetic drum rotation. A small proportion of cells responded during smooth tracking of a small spot of light. As a paradox to the physiological data, lesions of the uvula produced a profound effect on smooth-pursuit eye movements. Initial eye velocity for pursuit in the direction contraversive to the lesion site was increased substantially following lesions in comparison with prelesion controls. The lesions also affected optokinetic nystagmus in the direction contraversive to the lesion, but not as drastically as they did pursuit. Overall the results suggest that the uvula is not in the neuronal pathway that directly controls pursuit, but instead serves to adjust the gain of this system as a result of abnormal periods of motion of the visual world.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Angaut P, Brodal A (1967) The projection of the “vestibulocerebellum” onto the vestibular nuclei in the cat. Arch Ital Biol 105:441–479

    Google Scholar 

  • Baker JF, Petersen SE, Newsome WT, Allman JM (1981) Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): a quantitative comparison of medial, dorsomedial, dorsolateral, and middle temporal areas. J Neurophysiol 45:397–416

    Google Scholar 

  • Batton RR, Jayaraman A, Ruggiero D, Carpenter MB (1977) Fastigial efferent projections in the monkey: an autoradiographic study. J Comp Neurol 174:281–306

    Google Scholar 

  • Brodal P (1979) The pontocerebellar projection in the rhesus monkey: an experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4:193–208

    Google Scholar 

  • Brodal P (1982) Further observations on the cerebellar projections from the pontine nuclei and the nucleus reticularis tegmenti pontis in the rhesus monkey. J Comp Neurol 204:44–55

    Google Scholar 

  • Brodal A, Brodal P (1985) Observations on the secondary vestibulocerebellar projections in the macaque monkey. Exp Brain Res 58:62–74

    Google Scholar 

  • Büttner U, Waespe W (1981) Vestibular nerve activity in the alert monkey during vestibular and optokinetic nystagmus. Exp Brain Res 41:310–315

    Google Scholar 

  • Büttner U, Waespe W (1984) Purkinje cell activity in the primate flocculus during optokinetic stimulation, smooth pursuit eye movements, and VOR-suppression. Exp Brain Res 55:97–104

    Google Scholar 

  • Cannon SC, Robinson DA (1987) Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol 57:1383–1409

    CAS  PubMed  Google Scholar 

  • Cohen B, Matsuo V, Raphan T (1977) Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after nystagmus. J Physiol (Lond) 270:321–344

    Google Scholar 

  • Crandall WF, Keller EL (1985) Visual and oculomotor signals in nucleus reticularis tegmenti pontis in alert monkey. J Neurophysiol 54:1326–1345

    Google Scholar 

  • Fuchs AF, Robinson FR, Staube A (1994) Preliminary observations on the role of the caudal fastigial nucleus in the genration of smooth-pursuit eye movements. In: Fuchs AF, Brandt T, Büttner U, Zee DS (eds) Contemporary ocular motor and vestibular research: a tribute to David A. Robinson. Thieme, Stuttgart, pp 165–170

    Google Scholar 

  • Glickstein M, Gerrits N, Kralj-Hans I, Mercier B, Stein J, Voogd J (1994) Visual pontocerebellar projections in the macaque. J Comp Neurol 349:51–72

    Google Scholar 

  • Godaux E, Cheron G, Gravis F (1989) Eye movement evoked by microstimulation in the brainstem of the alert cat. Exp Brain Res 77:94–102

    Google Scholar 

  • Heinen S, Keller E (1992) Cerebellar uvula involvement in visual motion processing and smooth pursuit control in monkey. Ann NY Acad Sci 656:775–782

    Google Scholar 

  • Heinen SJ, Oh KD, Keller EL (1992) Characteristics of nystagmus evoked by electrical stimulation of the uvular/nodular lobules of the cerebellum in monkey. J Vestib Res 2:235–245

    Google Scholar 

  • Kase M, Miller DC, Noda H (1980) Discharges of Purkinje cells and mossy fibers in the cerebellar vermis of the monkey during saccadic eye movements and fixation. J Physiol (Lond) 300:539–555

    Google Scholar 

  • Keller EL (1988) Cerebellar involvement in smooth pursuit eye movement generation: flocculus and vermis. In: Kennard C, Clifford Rose F (eds) Physiological aspects of clinical neuroophthalmology. Chapman and Hall, London, pp 341–355

    Google Scholar 

  • Keller EL, Crandall WF (1983) Neuronal responses to optokinetic stimuli in pontine nuclei of behaving monkey. J Neurophysiol 49:169–187

    Google Scholar 

  • Keller EL, Heinen SJ (1991) Generation of smooth-pursuit eye movements: neuronal mechanisms and pathways. Neurosci Res 11:79–107

    Article  CAS  PubMed  Google Scholar 

  • Langer T, Fuchs AF, Chubb MC, Scudder CA, Lisberger SG (1985) Floccular efferents in the Rhesus macaque as revealed by auto-radiography and horseradish peroxidase. J Comp Neurol 235:26–37

    Google Scholar 

  • Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smoothpursuit eye movements and passive head rotation. J Neurophysiol 41:733–763

    Google Scholar 

  • McElligott JG, Keller EL (1982) Neuronal discharge in the posterior cerebellum: its relationship to saccadic eye movement generation. In: Lennerstrand G, Zee DS, Keller EL (eds) Functional basis of ocular motility disorders. Pergamon, Oxford, pp 453–461

    Google Scholar 

  • Miles FA (1991) The cerebellum. In: Carpenter RHS (ed) Eye movements. (Vision and visual dysfunction, vol 8). Macmillan, London, pp 224–243

    Google Scholar 

  • Miles FA, Fuller JH (1975) Visual tracking and the primate flocculus. Science 189:1000–1002

    Google Scholar 

  • Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273–299

    Google Scholar 

  • Miles FA, Fuller JH, Braitman DJ, Dow BM (1980) Long-term adaptive changes in primate vestibulo-ocular reflex. III. Electro-physiological observations in flocculus of normal monkey. J Neurophysiol 43:1437–1476

    Google Scholar 

  • Mustari MJ, Fuchs AF, Wallman J (1988) Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. J Neurophysiol 60:664–686

    Google Scholar 

  • Nagao S (1983) Effects of vestibulocerebellar lesions upon dynamic characteristics and adaptation of vestibulo-ocular and optokinetic responses in pigmented rabbits. Exp Brain Res 53:36–46

    Google Scholar 

  • Noda H, Fujikado T (1987) Involvement of Purkinje cells in evoking saccadic eye movements by microstimulation of the posterior cerebellar vermis of monkeys. J Neurophysiol 57:1247–1261

    Google Scholar 

  • Noda H, Suzuki DA (1979) The role of the flocculus of the monkey in saccadic eye movements. J Physiol Lond 294:317–334

    Google Scholar 

  • Noda H, Sugita S, Ikeda Y (1990) Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol 302:340–348

    Google Scholar 

  • Ohtsuka K, Noda H (1991) The effect of microstimulation of the oculomotor vermis on discharges of fastigial neurons and visually-directed saccades in macaques. Neurosci Res 10:290–295

    Google Scholar 

  • Optican LM, Robinson DA (1980) Cerebellar-dependendent adaptive control of primate saccadic system. J Neurophysiol 44:1058–1076

    Google Scholar 

  • Precht W, Simpson JI, Llinas R (1976) Responses of Purkinje cells in rabbit nodulus and uvula to natural vestibular and visual stimuli. Pflugers Arch 367:1–6

    Google Scholar 

  • Rashbass C (1961) The relationship between saccadic and smooth tracking eye movements. J Physiol (Lond) 159:326–338

    Google Scholar 

  • Richmond BJ, Optican LM, Podell M, Spitzer H (1987) Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. J Neurophysiol 57:132–146

    Google Scholar 

  • Stone LS, Lisberger SG (1990) Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J Neurophysiol 63:1241–1261

    Google Scholar 

  • Suzuki DA, Keller EL (1988a) The role of the middle vermis of monkey cerebellum in smooth-pursuit eye movement control. I. Eye and head movement-related activity. J Neurophysiol 59:1–18

    Google Scholar 

  • Suzuki DA, Keller EL (1988b) The role of the middle vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity. J Neurophysiol 59:19–40

    Google Scholar 

  • Suzuki DA, May JG, Keller EL, Yee RD (1990) Visual motion response properties of neurons in the dorsolateral pontine nucleus of the alert monkey. J Neurophysiol 63:37–59

    Google Scholar 

  • Thier P, Koehler W, Buettner UW (1988) Neuronal activity in the dorsolateral pontine nucleus of the alert monkey modulated by visual stimuli and eye movements. Exp Brain Res 70:496–512

    Google Scholar 

  • Voogd J, Bigaré F (1980) Topographical distribution of olivary and cortico nuclear fibers in the cerebellum: a review. In: Courville J, Montigny C de, Lamarre Y (eds) The inferior olivary nucleus. Raven, New York, pp 207–234

    Google Scholar 

  • Waespe W, Henn V (1977) Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 27:523–538

    Google Scholar 

  • Waespe W, Cohen B, Raphan T (1985) Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula. Science 228:199–202

    Google Scholar 

  • Zee DS (1982) Ocular motor control: the cerebellum. In: Lessell S, Dalen JTW van (eds) Neuro-ophthalmology. Excerpta Med, Amsterdam, pp 136–147

    Google Scholar 

  • Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effect of ablation of flocculus and paraflocculus on eye movement in primate. J Neurophysiol 46:878–899

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Smith-Kettlewell Eye Research Institute, 2232 Webster Street, 94115, San Francisco, CA, USA

    S. J. Heinen & E. L. Keller

Authors
  1. S. J. Heinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. L. Keller
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heinen, S.J., Keller, E.L. The function of the cerebellar uvula in monkey during optokinetic and pursuit eye movements: single-unit responses and lesion effects. Exp Brain Res 110, 1–14 (1996). https://doi.org/10.1007/BF00241368

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00241368

Key words

Search

Navigation