Skip to main content
SpringerLink
Log in

Influence of saccadic eye movements on geniculostriate excitability in normal monkeys

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Using permanently implanted electrodes in squirrel monkeys and macaques, transmission through the lateral geniculate nucleus (LGN) was assayed from the amplitude of potentials evoked in optic radiation by an electrical pulse applied to optic tract. Averaging of either individually or machine selected potentials, elicited at 0.3, 1.0, 20 or 50 Hz, in all cases showed a decrease in transmission ranging from 5–60 % in the period after saccadic eye movements made ad libitum. The suppression was greater in a patterned visual environment than in diffuse illumination, which in turn was greater than that occurring following saccades in the dark. Demonstration of the effect in darkness always required data averaging and never exceeded 20%. The effect was consistently greater in the magnocellular than parvocellular component. Suppression was often abruptly terminated and replaced by a facilitation of 5–15% about 100 msec after saccade detection. Comparable effects were observed for excitability of striate cortex tested by a stimulus pulse applied to optic radiation. In addition, sharply demarcated potentials inherently arising in LGN and striate cortex were found in association with saccades made even in total darkness. Neglecting a possible but dubious contribution from eye muscle proprioceptors, the experiments establish the existence of a centrally originating modulation of visual processing at both LGN and striate cortex in relation to saccadic eye movement in primates. This modulation may partially underlie the phenomenon of “saccadic suppression” and hasten the acquisition of a meaningful visual sample immediately following an ocular saccade. It remains uncertain as to how it may relate to similar or greater effects accompanying changes in alertness, or to fluctuations of unknown origin occurring sometimes semirhythmically at 0.05–0.03 Hz (Fig. 7).

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

  • Adey, W.R., Noda, H.: Influence of eye movements on geniculo-striate excitability in the cat. J. Physiol. (Lond.) 235, 805–821 (1973)

    Google Scholar 

  • Bartlett, J.R., Doty, R.W., Sr.: Influence of mesencephalic stimulation on unit activity in striate cortex of squirrel monkeys. J. Neurophysiol. 37, 642–652 (1974)

    Google Scholar 

  • Bartlett, J.R., Doty, R.W., Pecci-Saavedra, J., Wilson, P.D.: Mesencephalic control of lateral geniculate nucleus in primates. III. Modifications with state of alertness. Exp. Brain Res. 18, 214–224 (1973)

    Google Scholar 

  • Becker, W., Fuchs, A.F.: Further properties of the human saccade system: eye movements and correction saccades with and without visual fixation points. Vision Res. 9, 1247–1258 (1969)

    Google Scholar 

  • Becker, W., Hoehne, O., Iwase, K., Kornhuber, H.: Bereitschaftpotential, prämotorische Positivierung und andere Hirnpotentiale bei sakkadischen Augenbewegungen. Vision Res. 12, 421–436 (1972)

    Google Scholar 

  • Bizzi, E.: Discharge patterns of single geniculate neurons during the rapid eye movements of sleep. J. Neurophysiol. 29, 1087–1095 (1966)

    Google Scholar 

  • Bizzi, E., Brooks, D.C.: Functional connections between pontine reticular formation and lateral geniculate nucleus during deep sleep. Arch. ital. Biol. 101, 666–680 (1963)

    Google Scholar 

  • Brindley, G.S.: Sensory effects of electrical stimulation of the visual and paravisual cortex in man. In: Visual Centers in the Brain. Handbook of Sensory Physiology. Vol. VII/3B (ed. R. Jung), pp. 583–594. Berlin-Heidelberg-New York: Springer 1973

    Google Scholar 

  • Brindley, G.S., Merton, P.A.: The absence of position sense in the human eye. J. Physiol. (Lond.) 153, 127–130 (1960)

    Google Scholar 

  • Brooks, D.A., Gershon, M.D.: Eye movement potentials in the oculomotor and visual systems of the cat: a comparison of reserpine induced waves with those present during wakefulness and rapid eye movement sleep. Brain Res. 27, 223–239 (1971)

    Google Scholar 

  • Büttner, U., Fuchs, A.F.: Influence of saccadic eye movements on unit activity in simian lateral geniculate and pregeniculate nuclei. J. Neurophysiol. 36, 127–144 (1973)

    Google Scholar 

  • Chang, H.-T.: Cortical response to stimulation of the lateral geniculate body and the potentiation thereof by continuous illumination of retina. J. Neurophysiol. 15, 5–26 (1952)

    Google Scholar 

  • Cohen, B., Feldman, M.: Relationship of electrical activity in pontine reticular formation and lateral geniculate body to rapid eye movements. J. Neurophysiol. 31, 806–817 (1968)

    Google Scholar 

  • Cohen, B., Feldman, M.: Potential changes associated with rapid eye movements in the calcarine cortex. Exp. Neurol. 31, 100–113 (1971)

    Google Scholar 

  • Cohen, B., Komatsuzaki, A.: Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways. Exp. Neurol. 36, 101–117 (1972)

    Google Scholar 

  • Corazza, R., Lombroso, C.T.: The neuronal dark discharge during eye movements in awake “en- céphale isolé” cats. Brain Res. 34, 345–359 (1971)

    Google Scholar 

  • Dagnino, N., Favale, E., Loeb, C., Manfredi, M.: Sensory transmission in the geniculostriate system of the cat during natural sleep and arousal. J. Neurophysiol. 28, 443–456 (1965)

    Google Scholar 

  • Doty, R.W., Kimura, D.S., Mogenson, G.J.: Photically and electrically elicited responses in the central visual system of the squirrel monkey. Exp. Neurol. 10, 19–51 (1964)

    Google Scholar 

  • Doty, R.W., Lee, B.B., Bartlett, J.R., Sakakura, H.: Electrical excitability of primate central visual system following ocular saccades. Proc. Int. Union Physiol. Sci. 11, 221 (1974)

    Google Scholar 

  • Doty, R.W., Wilson, P.D., Bartlett, J.R., Pecci-Saavedra, J.: Mesencephalic control of lateral geniculate nucleus in primates. I. Electrophysiology. Exp. Brain Res. 18, 189–203 (1973)

    Google Scholar 

  • Duffy, F.H., Burchfiel, J.L.: Eye movement-related inhibition of primate visual neurons. Brain Res. 89, 121–132 (1975)

    Google Scholar 

  • Feldman, M., Cohen, B.: Electrical activity in the lateral geniculate body of alert monkey associated with eye movements. J. Neurophysiol. 31, 455–466 (1968)

    Google Scholar 

  • Fentress, J.F., Doty, R.W.: Effect of tetanization and enucleation upon excitability of visual pathways in squirrel monkeys and cats. Exp. Neurol. 30, 535–554 (1971)

    Google Scholar 

  • Gaarder, K.: Interpretive study of evoked responses elicited by gross saccadic eye movements. Percept. Motor Skills 27, 683–703 (1968)

    Google Scholar 

  • Gutman, J., Bergman, F., Chaimovitz, M., Costin, A.: Nystagmus evoked by stimulation of the optic pathways in the rabbit. Exp. Neurol. 8, 132–142 (1963)

    Google Scholar 

  • Haberich, F.J., Fischer, M.H.: Die Bedeutung des Lidschlags für das Sehen beim Umherblicken. flügers Arch. ges. Physiol. 267, 626–635 (1958)

    Google Scholar 

  • Hall, A.: The origin and purposes of blinking. Brit. J. Ophthal. 29, 445–467 (1945)

    Google Scholar 

  • Hobson, J.A., Alexander, J., Frederickson, C.J.: The effect of lateral geniculate lesions on phasic electrical activity of the cortex during desynchronized sleep in the cat. Brain Res. 14, 607–621 (1969)

    Google Scholar 

  • Holländer, H.: Projections from the striate cortex to the diencephalon in the squirrel monkey (Saimiri sciureus). A light microscopic radioautographic study following intracortical injection of H3 leucine. J. comp. Neurol. 155, 425–440 (1974)

    Google Scholar 

  • Holst, E. von, Mittelstaedt, H.: Das Reafferenzprinzip (Wechselwirkungen zwischen Zentralnervensystem und Peripherie). Naturwissenschaften 37, 464–476 (1950)

    Google Scholar 

  • Hörnsten, G., Högman, B., Örnberg, G.: Infrared methods for studying nystagmus and eye deviations in complete darkness with special reference to vertical nystagmus. Acta neurol. scand. 49, 511–524 (1973)

    Google Scholar 

  • Jeannerod, M.: Saccade correlated events in the lateral geniculate body. Bibl. ophthal. (Basel) 82, 189–198 (1972)

    Google Scholar 

  • Jeannerod, M., Chouvet, G.: Saccadic displacement of the retinal image: effects on the visual system in the cat. Vision Res. 13, 161–169 (1973)

    Google Scholar 

  • Kayama, Y., Riso, R.R., Bartlett, J.R., Doty, R.W., Sr.: Luxotonic units in striate cortex of alert macaques. Neurosci. Abstracts 1, 67 (1975)

    Google Scholar 

  • Kornmüller, A.E.: Eine experimentelle Anästhesie der äußeren Augenmuskeln am Menschen und ihre Auswirkungen. J. Psychol. Neurol. (Lpz.) 41, 354–366 (1931)

    Google Scholar 

  • Laurent, J.-P., Cespuglio, R., Jouvet, M.: Délimitation des voies ascendantes de l'activité pontogeniculo-occipitale chez le Chat. Brain Res. 65, 29–52 (1974)

    Google Scholar 

  • Laurent, J.-P., Guerrero, F.A., Jouvet, M.: Reversible suppression of the geniculate PGO waves and of the concomitant increase of excitability of the intrageniculate optic nerve terminals in cats. Brain Res. 81, 558–563 (1974)

    Google Scholar 

  • Le Gros Clark, W.E.: The laminar organization and cell content of the lateral geniculate body in the monkey. J. Anat. (Lond.) 75, 419–433 (1940–1941)

    Google Scholar 

  • Lynch, J.C., Yin, T.C.T., Talbot, W.H., Mountcastle, V.B.: A cortical source of command signals for visually evoked saccadic movements of the eyes in the monkey. Neurosci. Abstracts 1, 59 (1975)

    Google Scholar 

  • MacKay, D.M.: Visual stability and voluntary eye movements. In: Central Processing of Visual Information A: Integrative Functions and Comparative Data. Handbook of Sensory Physiology. Vol. VII/3A (ed. R. Jung), pp. 307–331. Berlin-Heidelberg-New York: Springer 1973

    Google Scholar 

  • Matin, E.: Saccadic suppression: a review and an analysis. Psychol. Bull. 81, 899–917 (1974)

    Google Scholar 

  • Meulders, M., Godfraind, J.M.: Influence du réveil d'origine réticulaire sur l'étendue des champs visuels des neurones de la region genouillée chez la Chat avec cerveau intact ou avec cerveau isolé. Exp. Brain Res. 9, 201–220 (1969)

    Google Scholar 

  • Mitrani, L., Radil-Weiss, T., Yakimoff, N., Mateeff, St., Bozkov, V.: Deterioration of vision due to contour shift over the retina during eye movements. Vision Res. 15, 877–878 (1975)

    Google Scholar 

  • Munson, J.B., Schwartz, K.S.: Lateral geniculate and occipital cortex spikes with eye movements in awake and sleeping cats: temporal and functional correlations. Exp. Neurol. 35, 300–304 (1972)

    Google Scholar 

  • Munson, J.B., Van Hartesveldt, C.J., Spray, D.C.: Graded, unitary and eye movement potentials in lateral geniculate nucleus following reticular stimulation. Vision Res. 15, 443–446 (1975)

    Google Scholar 

  • Noda, H.: Depression in the excitability of relay cells of lateral geniculate nucleus following saccadic eye movements in the cat. J. Physiol. (Lond.) 249, 87–102 (1975)

    Google Scholar 

  • Orban, G., Vandenbussche, E., Callens, M.: Electrophysiological evidence for the existence of connections between the brain stem oculomotor areas and the visual system in the cat. Brain Res. 41, 225–229 (1972)

    Google Scholar 

  • Riggs, L.A., Merton, P.A., Morton, H.B.: Suppression of visual phosphenes during saccadic eye movements. Vision Res. 14, 997–1011 (1974)

    Google Scholar 

  • Robinson, D.L., Wurtz, R.H.: Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movement. J. Neurophysiol. (in press, 1976)

  • Sakai, K.: Phasic electrical activity in the brain associated with eye movement in waking cats. Brain Res. 56, 135–150 (1973)

    Google Scholar 

  • Sakakura, H., Doty, R.W., Sr.: EEG of striate cortex in blind monkeys: effects of eye movements and sleep. Arch. ital. Biol. 114, 23–48 (1976)

    Google Scholar 

  • Schwartzbaum, J.S.: Interrelationship among multiunit activity of the midbrain reticular formation and lateral geniculate nucleus, thalamocortical arousal, and behavior in rats. J. comp. physiol. Psychol. 89, 131–157 (1975)

    Google Scholar 

  • Sharpe, C.R.: The visibility and fading of thin lines visualized by their controlled movement across the retina. J. Physiol. (Lond.) 222, 113–134 (1972)

    Google Scholar 

  • Singer, W., Bedworth, N.: Correlation between the effects of brain stem stimulation and saccadic eye movements on transmission in the cat lateral geniculate nucleus. Brain Res. 72, 185–202 (1974)

    Google Scholar 

  • Skavenski, A.A., Robinson, D.A.: Role of abducens neurons in vestibulocular reflex. J. Neurophysiol. 36, 724–738 (1973)

    Google Scholar 

  • Sperry, R.: Neural basis of spontaneous optokinetic response produced by visual inversion. J. comp. physiol. Psychol. 43, 482–489 (1950)

    Google Scholar 

  • Valleala, P.: Nystagmus and the activity of visual cortex cells. Experientia (Basel) 24, 358–359 (1968)

    Google Scholar 

  • Vital-Durand, F., Jeannerod, M.: Eye movement related activity in the visual cortex of darkreared kittens. E.E.G. clin. Neurophysiol. 38, 295–301 (1975)

    Google Scholar 

  • Walsh, J.T., Cordeau, J.P.: Responsiveness in the visual system during various phases of sleep and waking. Exp. Neurol. 11, 80–103 (1965)

    Google Scholar 

  • Wilson, P.D., Pecci-Saavedra, J., Doty, R.W.: Mesencephalic control of lateral geniculate nucleus in primates. II. Effective loci. Exp. Brain Res. 18, 201–213 (1973)

    Google Scholar 

  • Wurtz, R.H.: Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. J. Neurophysiol. 32, 987–994 (1969)

    Google Scholar 

  • Yarbus, A.L.: Eye Movements and Vision. Translated by B. Haigh. (ed. L.A. Riggs). 222 pp. New York: Plenum 1967

    Google Scholar 

  • Yin, T.C.T., Lynch, J.C., Talbot, W.H., Mountcastle, V.B.: Neuronal mechanisms of the parietal lobe for directed visual attention studied in waking monkeys. Neurosci. Abstracts 1, 59 (1975)

    Google Scholar 

Download references

Author information

Author notes

  1. B. B. Lee

    Present address: Max-Planck-Institut für Biophysikalische Chemie, Karl-Friedrich-Bonhoeffer-Institut, Göttingen-Nikolausberg, Germany

  2. H. Sakakura

    Present address: Department of Psychiatry, Sumitomo Hospital, Osaka, Japan

Authors and Affiliations

  1. Center for Brain Research, University of Rochester, 14642, Rochester, New York, USA

    J. R. Bartlett, R. W. Doty,  B. B. Lee & H. Sakakura

Authors
  1. J. R. Bartlett
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. W. Doty
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. B. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. Sakakura
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by Grant NS 03606 and Contract 70-2279 from the National Institutes of Neurological Diseases and Stroke, National Institutes of Health and by Grant GB 7522X from the National Science Foundation. B.B.L. was also aided by a travel grant from the Wellcome Trust (U.K.) and H.S. received a travel grant from the International Brain Research Organization.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bartlett, J.R., Doty, R.W., Lee, B.B. et al. Influence of saccadic eye movements on geniculostriate excitability in normal monkeys. Exp Brain Res 25, 487–509 (1976). https://doi.org/10.1007/BF00239783

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00239783

Key words

Search

Navigation