Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-23T11:36:40.308Z Has data issue: false hasContentIssue false
  • English
  • Français

A model for optokinetic eye movements in turtles that incorporates properties of retinal-slip neurons

Published online by Cambridge University Press:  02 June 2009

Alexander F. Rosenberg  and
Michael Ariel
Alexander F. Rosenberg
Affiliation:
Department of Behavioral Neuroscience, University of Pittsburgh, Pittsburgh
Michael Ariel
Affiliation:
Department of Behavioral Neuroscience, University of Pittsburgh, Pittsburgh Department of Ophthalmology and Psychiatry, University of Pittsburgh, Pittsburgh
Get access Rights & Permissions [Opens in a new window]

Abstract

The turtle's optokinetic response is described by a simple model that incorporates visual-response properties of neurons in the pretectum and accessory optic system. Using data from neuronal and eye-movement recordings that have been previously published, the model was realized using algebraic-block simulation software. It was found that the optokinetic response, modelled as a simple negative feedback system, was similar to that measured from a behaving animal. Because the responses of retinal-slip detecting neurons corresponded to the nonlinear, closed-loop optokinetic response, it was concluded that the visual signals encoded in these neurons could provide sufficient sensory information to drive the optokinetic reflex. Furthermore, it appears that the low gain of optokinetic eye movements in turtles, which have a negligible velocity storage time constant, may allow stable oculomotor output in spite of neuronal delays in the reflex pathway. This model illustrates how visual neurons in the pretectum and accessory optic system can contribute to visually guided eye movements.

Keywords

Accessory optic systemPretectumOptokineticOculomotorTurtle
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 375 - 383
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ariel, M. (1990). Independent eye movements in the turtle. Visual Neuroscience 5, 29–41.CrossRefGoogle ScholarPubMed
Bass, A. & Northcutt, G. (1981). Retinal recipient nuclei in the painted turtle, chrysemys picta: An autoradiographic study. Journal of Comparative Neurology 199, 97–112.CrossRefGoogle Scholar
Burns, S. & Wallman, J. (1981). Relation of single unit properties to the oculomotor function of the nucleus of the basal optic root (accessory optic system) in chickens. Experimental Brain Research 42, 171–180.CrossRefGoogle Scholar
Cohen, B., Matsuo, V. & Raphan, T. (1977). Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. Journal of Physiology (London) 270, 321–344.CrossRefGoogle ScholarPubMed
Collewijn, H. (1969). Optokinetic eye movements in the rabbit: Input-output relations. Vision Research 9, 117–132.CrossRefGoogle ScholarPubMed
Collewijn, H. (1972). An analog model of the rabbit's optokinetic system. Brain Research 36, 71–88.CrossRefGoogle ScholarPubMed
Collewijn, H. (1975 a). Direction selective units in the rabbit's nucleus of the optic tract. Brain Research 100, 489–508.CrossRefGoogle ScholarPubMed
Collewijn, H. (1975 b). Oculomotor areas in the rabbit's midbrain and pretectum. Journal of Neurobiology 6, 3–22.CrossRefGoogle ScholarPubMed
Dieringer, N., Cochran, S.L. & Precht, W. (1983). Differences in the central organization of gaze stabilizing reflexes between frog and turtle. Brain, Behavior, and Evolution 153, 495–508.Google Scholar
Dieringer, N., Reichenberger, I. & Graf, W. (1992). Differences in optokinetic and vestibular ocular reflex performance in teleosts and their relationship to different life styles. Brain, Behavior, and Evolution 39, 289–304.CrossRefGoogle ScholarPubMed
Fan, T.X., Weber, A.E., Pickard, G.E., Faber, K.M. & Ariel, M. (1995). Visual responses and connectivity in the turtle pretectum. Journal of Neurophysiology 73, 2507–2521.CrossRefGoogle ScholarPubMed
Gioanni, H., Rey, J., Villalobos, J., Bouyer, J.J. & Gioanni, Y. (1981). Optokinetic nystagmus in the pigeon (Columba livia). I. Study in monocular and binocular vision. Experimental Brain Research 44, 362–370.CrossRefGoogle ScholarPubMed
Gioanni, H., Rey, J., Villalobos, J., Richard, D. & Dalbera, A. (1983). Optokinetic nystagmus in the pigeon (Columba livia). II. Role of the pretectal nucleus of the accessory optic system (AOS). Experimental Brain Research 50, 237–247.Google ScholarPubMed
Grasse, K.L. & Cynader, M. (1982). Electrophysiology of medial terminal nucleus of accessory optic system in the cat. Journal of Neurophysiology 48, 490–504.CrossRefGoogle ScholarPubMed
Grasse, K.L. & Cynader, M. (1984). Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system. Journal of Neurophysiology 51, 276–293.CrossRefGoogle ScholarPubMed
Grasse, K.L., Cynader, M. & Douglas, R. (1984). Alterations in response properties in the lateral and dorsal terminal nuclei of the cat accessory optic system following visual cortex lesions. Experimental Brain Research 55, 69–80.CrossRefGoogle ScholarPubMed
Hein, A., Courjon, J.H., Flandrin, J.M. & Arzi, M. (1990). Optokinetic nystagmus in the ferret: including selected comparisons with the cat. Experimental Brain Research 79, 623–632.CrossRefGoogle ScholarPubMed
Hess, B.J.M., Precht, W., Reber, A. & Cazin, L. (1985). Horizontal optokinetic ocular nystagmus in the pigmented rat. Neuroscience 15, 97–107.CrossRefGoogle ScholarPubMed
Hoffmann, K.P. & Distler, C. (1989). Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. Journal of Neurophysiology 62, 416–428.CrossRefGoogle ScholarPubMed
Hoffmann, K.P. & Schoppmann, A. (1981). A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract. Experimental Brain Research 42, 146–157.CrossRefGoogle ScholarPubMed
Kato, I., Harada, K., Hasegawa, T., Igarashi, T., Koike, Y. & Kawasaki, T. (1986). Role of the nucleus of the optic tract in monkeys in relation to optokinetic nystagmus. Brain Research 364, 12–22.CrossRefGoogle ScholarPubMed
Maioli, C. & Precht, W. (1984). The horizontal optokinetic nystagmus in the cat. Experimental Brain Research 55, 494–506.CrossRefGoogle ScholarPubMed
Manteuffel, G. (1984). A ‘physiological’ model for the salamander horizontal optokinetic reflex. Brain, Behavior, and Evolution 25, 197–205.CrossRefGoogle ScholarPubMed
Manteuffel, G., Kopp, J. & Himstedt, W. (1986). Amphibian optokinetic afternystagmus: Properties and comparative analysis in various species. Brain, Behavior, and Evolution 28, 186–197.CrossRefGoogle Scholar
McKenna, O.C. & Wallman, J. (1985). The accessory optic system and pretectum of birds: Comparisons with those of other vertebrates. Brain, Behavior, and Evolution 26, 91–116.CrossRefGoogle ScholarPubMed
Mustari, M.J. & Fuchs, A.F. (1990). Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate. Journal of Neurophysiology 64, 77–90.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1981). The use of control systems analysis in the neurophysiology of eye movements. Annual Review of Neuroscience 4, 463–503.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1987). Why visuomotor systems don't like negative feedback and how they avoid it. In Vision, Brain and Cooperative Computation, ed. Arbib, M.A. & Hanson, A.R., pp. 89–107. Cambridge, Massachusetts: MIT Press.CrossRefGoogle Scholar
Rosenberg, A.F. & Ariel, M. (1990). Visual-response properties of neurons in turtle basal optic nucleus in vitro. Journal of Neurophysiology 63, 1033–1045.CrossRefGoogle ScholarPubMed
Schiff, D., Cohen, B., Buttner-Ennever, J. & Matsuo, V. (1990). Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and after-nystagmus in the monkey. Experimental Brain Research 79, 225–239.CrossRefGoogle ScholarPubMed
Schiff, D., Cohen, B. & Raphan, T. (1988). Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey. Experimental Brain Research 70, 1–14.CrossRefGoogle ScholarPubMed
Simpson, J.I., Giolli, R.A. & Blanks, R.H.I. (1988). The pretectal nuclear complex and the accessory optic system. In: Neuroanatomy of the Oculomotor System, ed. Buttner-Ennever, J., pp. 335–364. Amsterdam: Elsevier.Google Scholar
Soodak, R.E. & Simpson, J.I. (1988). The accessory optic system of rabbit: I. Basic visual response properties. Journal of Neurophysiology 60, 2037–2054.CrossRefGoogle ScholarPubMed
Tijssen, M.A., Hain, T.C., Straathof, C.S.M. & Zee, D.S. (1989). Optokinetic afternystagmus in humans: Normal values of amplitude, time constant, and symmetry. Annals of Otology, Rhinology and Laryngology 98, 741–746.CrossRefGoogle Scholar
Waespe, W. & Henn, V. (1977). Vestibular nuclei activity during optokinetic after-nystagmus (OKAN) in the alert monkey. Experimental Brain Research 30, 323–330.Google ScholarPubMed
Wallman, J., McKenna, O.C., Burns, S., Velez, J. & Weinstein, B. (1981). Relation of the accessory optic system and pretectum to optokinetic responses in chickens. In Progress in Oculomotor Research, ed. Fuchs, A.F. & Becker, W., pp. 437–442. Amsterdam: Elsevier.Google Scholar
Wallman, J. (1993). Subcortical optokinetic mechanisms. In Visual Motion and its Role in the Stabilization of Gaze, ed. Miles, F.A. & Wallman, J., pp. 321–342. Amsterdam: Elsevier.Google Scholar