Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-27T03:32:31.037Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphology of the turtle accessory optic system

Published online by Cambridge University Press:  30 March 2004

JOHN MARTIN ,
NAOKI KOGO ,
TIAN XING FAN  and
MICHAEL ARIEL
JOHN MARTIN
Affiliation:
Department of Anatomy and Neurobiology, Saint Louis University School of Medicine, Saint Louis
NAOKI KOGO
Affiliation:
Department of Anatomy and Neurobiology, Saint Louis University School of Medicine, Saint Louis Current address: Department of Elektrotechniek, Katholieke Universiteit Lueven, Kasteelpark Arenberg 10, B-3001, Heverlee, Belgium
TIAN XING FAN
Affiliation:
Department of Anatomy and Neurobiology, Saint Louis University School of Medicine, Saint Louis
MICHAEL ARIEL
Affiliation:
Department of Anatomy and Neurobiology, Saint Louis University School of Medicine, Saint Louis
Get access Rights & Permissions [Opens in a new window]

Abstract

Neural signals of the moving visual world are detected by a subclass of retinal ganglion cells that project to the accessory optic system in the vertebrate brainstem. We studied the dendritic morphologies and direction tuning of these brainstem neurons in turtle (Pseudemys scripta elegans) to understand their role in visual processing. Full-field checkerboard patterns were drifted on the contralateral retina while whole-cell recordings were made in the basal optic nucleus in an intact brainstem preparation in vitro. Neurobiotin diffused into the neurons during the recording and was subsequently localized in brain sections. Neuronal morphologies were traced using appropriate computer software to analyze their position in the brainstem. Most labeled neurons were fusiform in shape and had numerous varicosities along their processes. The majority of dendritic trees spread out in a transverse plane perpendicular to the rostrocaudal axis of the nucleus. Neurons near the brainstem surface were often oriented tangential to that surface, whereas more cells at the dorsal side of the nucleus were oriented radial to the brainstem surface. Further analysis of Nissl-stained neurons revealed the largest neurons are located in the rostral and medial portions of the nucleus although neurons are most densely packed in the middle of the nucleus. The preferred directions of the visual responses of the neurons in this sample did not correlate with their morphology and position in the nucleus. Therefore, the morphology of the cells in the turtle accessory optic system appears dependent on its position within the nucleus while its visual responses may depend on the synaptic inputs that contact each cell.

Keywords

Basal optic nucleusDirection-sensitive cellsWhole-cell recordingsNeurobiotinNissl staining
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 6 , November 2003 , pp. 639 - 649
Copyright
© 2003 Cambridge University Press

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

REFERENCES

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 239–247.Google Scholar
Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.Google Scholar
Amthor, F.R. & Oyster, C.W. (1995). Spatial organization of retinal information about the direction of image motion. Proceedings of the National Academy of Sciences of the U.S.A. 92, 4002–4005.Google Scholar
Ariel, M. & Rosenberg, A.F. (1991). Effects of synaptic drugs on turtle optokinetic nystagmus and the spike responses of the basal optic nucleus. Visual Neuroscience 7, 431–440.Google Scholar
Ariel, M. & Kogo, N. (2001). Direction tuning of inhibitory inputs to the turtle accessory optic system. Journal of Neurophysiology 86, 2919–2930.Google Scholar
Blanks, R.H., Giolli, R.A., & Pham, S.V. (1982). Projections of the medial terminal nucleus of the accessory optic system upon pretectal nuclei in the pigmented rat. Experimental Brain Research 48, 228–237.Google Scholar
Brecha, N. & Karten, H.J. (1979). Accessory optic projections upon oculomotor nuclei and vestibulocerebellum. Science 203, 913–916.Google Scholar
Brecha, N., Karten, H.J., & Hunt, S.P. (1980). Projections of the nucleus of the basal optic root in the pigeon: An autoradiographic and horseradish peroxidase study. Journal of Comparative Neurology 189, 615–670.Google 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.Google Scholar
Cochran, S.L., Dieringer, N., & Precht, W. (1984). Basic optokinetic-ocular reflex pathways in the frog. Journal of Neuroscience 4, 43–57.Google Scholar
Fite, K.V., Reiner, A., & Hunt, S.P. (1979). Optokinetic nystagmus and the accessory optic system of pigeon and turtle. Brain, Behavior and Evolution 16, 192–202.Google Scholar
Fite, K.V., Bengston, L.C., & Montgomery, N.M. (1988). Anuran accessory optic system: Evidence for a dual organization. Journal of Comparative Neurology 273, 377–384.Google Scholar
Gioanni, H., Villalobos, J., Rey, J., & Dalbera, A. (1983). Optokinetic nystagmus in the pigeon (Columba livia). III. Role of the nucleus ectomamillaris (nEM): Interactions in the accessory optic system (AOS). Experimental Brain Research 50, 248–258.Google Scholar
Giolli, R.A., Braithwaite, J.R., & Streeter, T.T. (1968). Golgi study of the nucleus of the transpeduncular tract in the rabbit. Journal of Comparative Neurology 133, 309–328.Google Scholar
Gregory, K.M. & Giolli, R.A. (1985). The dendritic architecture of the medial terminal nucleus of the accessory optic system in the rat, rabbit, and cat. Experimental Brain Research 60, 501–508.Google Scholar
Kogo, N. & Ariel, M. (1997). Membrane properties and monosynaptic retinal excitation of neurons in the turtle accessory optic system. Journal of Neurophysiology 78, 614–627.Google Scholar
Kogo, N., Rubio, D.M., & Ariel, M. (1998). Direction tuning of individual retinal inputs to the turtle accessory optic system. Journal of Neuroscience 18, 2673–2684.Google Scholar
Lazar, G. (1983). Transection of the basal optic root in the frog abolishes vertical optokinetic head-nystagmus. Neuroscience Letters 43, 7–11.Google Scholar
Martin, J., Kogo, N., & Ariel, M. (1998). Morphology of basal optic tract terminals in the turtle, Pseudemys scripta elegans. Journal of Comparative Neurology 393, 267–283.Google Scholar
McKenna, O.C. & Wallman, J. (1981). Identification of avian brain regions responsive to retinal slip using 2-deoxyglucose. Brain Research 210, 455–460.Google Scholar
McKenna, O.C. & Wallman, J. (1985a). Accessory optic system and pretectum of birds: Comparisons with those of other vertebrates. Brain, Behavior and Evolution 26, 91–116.Google Scholar
McKenna, O.C. & Wallman, J. (1985b). Functional postnatal changes in avian brain regions responsive to retinal slip: A 2-deoxy-D-glucose study. Journal of Neuroscience 5, 330–342.Google Scholar
Mesulam, M.M. (1978). Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106–117.Google Scholar
Montgomery, N., Fite, K.V., & Bengston, L. (1981). The accessory optic system of Rana pipiens: Neuroanatomical connections and intrinsic organization. Journal of Comparative Neurology 203, 595–612.Google Scholar
Northmore, D.P. & Granda, A.M. (1991). Ocular dimensions and schematic eyes of freshwater and sea turtles. Visual Neuroscience 7, 627–635.Google Scholar
Reiner, A. & Karten, H.J. (1978). A bisynaptic retinocerebellar pathway in the turtle. Brain Research 150, 163–169.Google Scholar
Reiner, A., Brecha, N., & Karten, H.J. (1979). A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4, 1679–1688.Google 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.Google Scholar
Rosenberg, A.F. & Ariel, M. (1991). Electrophysiological evidence for a direct projection of direction-sensitive retinal ganglion cells to the turtle's accessory optic system. Journal of Neurophysiology 65, 1022–1033.Google Scholar
Rosenberg, A.F. & Ariel, M. (1998). Analysis of direction-tuning curves of neurons in the turtle's accessory optic system. Experimental Brain Research 121, 361–370.Google Scholar
Schmidt, M., Vandertogt, C., Wahle, P., & Hoffmann, K.P. (1998). Characterization of a directional selective inhibitory input from the medial terminal nucleus to the pretectal nuclear complex in the rat. European Journal of Neuroscience 10, 1533–1543.Google Scholar
Schuerger, R.J., Rosenberg, A.F., & Ariel, M. (1990). Retinal direction-sensitive input to the accessory optic system: An in vitro approach with behavioral relevance. Brain Research 522, 161–164.Google Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.Google Scholar
van der Togt, C., van der Want, J., & Schmidt, M. (1993). Segregation of direction selective neurons and synaptic organization of inhibitory intranuclear connections in the medial terminal nucleus of the rat: An electrophysiological and immunoelectron microscopical study. Journal of Comparative Neurology 338, 175–192.Google Scholar
Wallman, J. & Velez, J. (1985). Directional asymmetries of optokinetic nystagmus: Developmental changes and relation to the accessory optic system and to the vestibular system. Journal of Neuroscience 5, 317–329.Google Scholar
Woodbury, P.B. & Ulinski, P.S. (1986). Conduction velocity, size and distribution of optic nerve axons in the turtle, Pseudemys scripta elegans. Anatomy and Embryology 174, 253–263.Google Scholar
Wylie, D.R. & Frost, B.J. (1990). Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow. Visual Neuroscience 5, 489–495.Google Scholar
Zhang, D. & Eldred, W.D. (1994). Anatomical characterization of retinal ganglion cells that project to the nucleus of the basal optic root in the turtle (Pseudemys scripta elegans). Neuroscience 61, 707–718.Google Scholar