Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-24T20:18:57.911Z Has data issue: false hasContentIssue false
  • English
  • Français

Pupil constriction evoked in vitro by stimulation of the oculomotor nerve in the turtle (Trachemys scripta elegans)

Published online by Cambridge University Press:  01 May 2009

JAMES R. DEARWORTH JR ,
J.E. BRENNER ,
J.F. BLAUM ,
T.E. LITTLEFIELD ,
D.A. FINK ,
J.M. ROMANO  and
M.S. JONES
JAMES R. DEARWORTH JR*
Affiliation:
Department of Biology and Neuroscience Program, Lafayette College, Easton, Pennsylvania
J.E. BRENNER
Affiliation:
Department of Biology and Neuroscience Program, Lafayette College, Easton, Pennsylvania
J.F. BLAUM
Affiliation:
Department of Biology and Neuroscience Program, Lafayette College, Easton, Pennsylvania
T.E. LITTLEFIELD
Affiliation:
Department of Biology and Neuroscience Program, Lafayette College, Easton, Pennsylvania
D.A. FINK
Affiliation:
Department of Biology and Neuroscience Program, Lafayette College, Easton, Pennsylvania
J.M. ROMANO
Affiliation:
Department of Biology and Neuroscience Program, Lafayette College, Easton, Pennsylvania
M.S. JONES
Affiliation:
Department of Pharmacological & Physiological Science, Saint Louis University School of Medicine, Saint Louis, Missouri
*
*Address correspondence and reprint requests to: James R. Dearworth JR., Department of Biology and Neuroscience Program, Lafayette College, Easton, PA 18042-1778. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The pond turtle (Trachemys scripta elegans) exhibits a notably sluggish pupillary light reflex (PLR), with pupil constriction developing over several minutes following light onset. In the present study, we examined the dynamics of the efferent branch of the reflex in vitro using preparations consisting of either the isolated head or the enucleated eye. Stimulation of the oculomotor nerve (nIII) using 100-Hz current trains resulted in a maximal pupil constriction of 17.4% compared to 27.1% observed in the intact animal in response to light. When current amplitude was systematically increased from 1 to 400 μA, mean response latency decreased from 64 to 45 ms, but this change was not statistically significant. Hill equations fitted to these responses indicated a current threshold of 3.8 μA. Stimulation using single pulses evoked a smaller constriction (3.8%) with response latencies and threshold similar to that obtained using train stimulation. The response evoked by postganglionic stimulation of the ciliary nerve using 100-Hz trains was largely indistinguishable from that of train stimulation of nIII. However, application of single-pulse stimulation postganglionically resulted in smaller pupil constriction at all current levels relative to that of nIII stimulation, suggesting that there is amplification of efferent drive at the ganglion. Time constants for constrictions ranged from 88 to 154 ms with relaxations occurring more slowly at 174–361 ms. These values for timing from in vitro are much faster than the time constant 1.66 min obtained for the light response in the intact animal. The rapid dynamics of pupil constriction observed here suggest that the slow PLR of the turtle observed in vivo is not due to limitations of the efferent pathway. Rather, the sluggish response probably results from photoreceptive mechanisms or central processing.

Keywords

TurtlePupilOculomotorIn vitroTime constant
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 309 - 318
Copyright
Copyright © Cambridge University Press 2009

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

Berson, D.M., Dunn, F.A. & Takao, M. (2002). Phototransduction by retinal ganglion cells that set the circadian clock. Science 295, 1070–1073.CrossRefGoogle ScholarPubMed
Brown, K.T. (1969). A linear area centralis extending across the turtle retina and stabilized to the horizon by non-visual cues. Vision Research 9, 1053–1062.CrossRefGoogle Scholar
Clarke, R.J. (2007). Shaping the pupil’s response to light in the hooded rat. Experimental Brain Research 176, 641–651.CrossRefGoogle ScholarPubMed
Dearworth, J.R. & Cooper, L.J. (2008). Sympathetic influence on the pupillary light response in three red-eared slider turtles (Trachemys scripta elegans). Veterinary Ophthalmology 11, 306–313.CrossRefGoogle ScholarPubMed
Dearworth, J.R., Cooper, L.J. & McGee, C. (2007). Parasympathetic control of the pupillary light response in the red-eared slider turtle (Pseudemys scripta elegans). Veterinary Ophthalmology 10, 106–110.CrossRefGoogle ScholarPubMed
Dvorak, C.A., Granda, A.M. & Maxwell, J.H. (1980). Photoreceptor signals at visual threshold. Nature 283, 860–861.CrossRefGoogle ScholarPubMed
Fan, T.X., Scudder, C. & Ariel, M. (1997). Neuronal responses to turtle head rotation in vitro. Journal of Neurobiology 33, 99–117.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Frigato, E., Vallone, D., Bertolucci, C. & Foulkes, N.S. (2006). Isolation and characterization of melanopsin and pinopsin expression within photoreceptive sites of reptiles. Die Naturwissenschaften 93, 379–385.CrossRefGoogle ScholarPubMed
Gamlin, P.D.R. (2000). Functions of the Edinger-Westphal nucleus. In Nervous Control of the Eye, ed. Burnstock, G. & Sillito, A.M., pp. 117–255. Amsterdam, The Netherlands: Harwood academic publishers.Google Scholar
Gamlin, P.D.R. (2005). The pretectum: Connections and oculomotor-related roles. Progress in Brain Research 151, 379–405.CrossRefGoogle Scholar
Gamlin, P.D., McDougal, D.H., Pokorny, J., Smith, V.C., Yau, K.-W. & Dacey, D.M. (2007). Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Research 47, 946–954.CrossRefGoogle ScholarPubMed
Granda, A.M., Dearworth, J.R. Jr, Kittila, C.A. & Boyd, W.D. (1995). The pupillary response to light in the turtle. Visual Neuroscience 12, 1127–1133.CrossRefGoogle ScholarPubMed
Hultborn, H., Mori, K. & Tsukahara, N. (1978). Cerebellar influence on parasympathetic neurones innervating intra-ocular muscles. Brain Research 159, 269–278.CrossRefGoogle ScholarPubMed
Iske, M.S. (1929). A study of the iris mechanism of the alligator. Anatomical Record 44, 57–77.CrossRefGoogle Scholar
Jampel, R.S. (1962). Extraocular muscle action from brain stimulation in the macaque. Investigative Ophthalmology 1, 565–578.Google ScholarPubMed
Jones, M.S. & Ariel, M. (2008). Morphology, intrinsic membrane properties, and rotation-evoked responses of trochlear motoneurons in the turtle. Journal of Neurophysiology 99, 1187–1200.CrossRefGoogle Scholar
Kardon, R.H. (2005). Anatomy and physiology of the autonomic nervous system. In Wash and Hoyt’s Clinical Neuro-Ophthalmology (6th ed.), ed. Miller, N.R., Newman, N.J., Biousse, V. & Kerrison, J.B., pp. 649–714. Baltimore, MD: Lipponcott Williams & Wilkins.Google Scholar
Keifer, J. & Houk, J.C. (1991). Role of excitatory amino acids in mediating burst discharge of red nucleus neurons in the in vitro turtle brain stem-cerebellum. Journal of Neurophysiology 65, 454–467.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Loerzel, S.M., Smith, P.J., Howe, A. & Samuelson, D.A. (2002). Vecuronium bromide, phenylephrine and atropine combinations as mydriatics in juvenile double-crested cormorants (phalacrocorax auritus). Veterinary Ophthalmology 5, 149–154.CrossRefGoogle ScholarPubMed
Loewenfeld, I.E. (1958). Mechanisms of reflex dilatation of the pupil. Documenta Ophthalmologica. Advances in Opthalmology 12, 185–448.CrossRefGoogle Scholar
Loewenfeld, I.E. (1993). The Pupil—Anatomy, Physiology, and Clinical Applications. Vol. I.; and Bibliography and Index. Vol. II. Detroit, MI: Wayne State University Press.Google Scholar
Lowenstein, O. & Loewenfeld, I.E. (1950 a). Role of sympathetic and parasympathetic systems in reflex dilatation of the pupil: Pupillographic studies. Archives of Neurology and Psychiatry 64, 313–340.CrossRefGoogle Scholar
Lowenstein, O. & Loewenfeld, I.E. (1950 b). Mutual role of sympathetic and parasympathetic in shaping of the pupillary reflex to light: Pupillographic studies. Archives of Neurology and Psychiatry 64, 341–377.CrossRefGoogle ScholarPubMed
Lucas, R.J., Douglas, R.H. & Foster, R.G. (2001). Characterization of a novel ocular photopigment capable of driving pupillary constriction in mice. Nature Neuroscience 4, 621–626.CrossRefGoogle Scholar
Lutz, P.L. & Milton, S.L. (2004). Negotiating brain anoxia survival in the turtle. The Journal of Experimental Biology 207, 3141–3147.CrossRefGoogle ScholarPubMed
Maxwell, J.H. (1979). Anesthesia and surgery. In Turtles: Perspective and Research, ed. Harless, M. & Morlock, H., pp. 127–152. New York: Wiley.Google Scholar
McDougal, D.H. & Gamlin, P.D.R. (2008). Pupillary control pathways. In The Senses: A Comprehensive Reference, Vol. 1, Vision I, ed. Masland, R.H., Albright, T.D., Basbaum, A.I., Shepherd, G.M. & Westheimer, G.,pp. 521–536. San Diego, CA: Academic Press.CrossRefGoogle Scholar
Nisida, I., Okada, H. & Nakano, O. (1960). The activity of the ciliospinal centers and their inhibition in pupillary light reflex. The Japanese Journal of Physiology 10, 73–84.CrossRefGoogle ScholarPubMed
Northmore, D.P.M. & Granda, A.M. (1991). Ocular dimensions and schematic eyes of freshwater and sea turtles. Visual Neuroscience 7, 627–635.CrossRefGoogle ScholarPubMed
Passatore, M. & Pettorossi, V.E. (1976). Efferent fibers in the cervical sympathetic nerve influenced by light. Experimental Neurology 52, 66–82.CrossRefGoogle ScholarPubMed
Pilar, G. & Vaughan, P.C. (1969 a). Electrophysiological investigations of the pigeon iris neuromuscular junctions. Comparative Biochemistry and Physiology 29, 51–72.CrossRefGoogle ScholarPubMed
Pilar, G. & Vaughan, P.C. (1969 b). Mechanical responses of the pigeon iris muscle fibers. Comparative Biochemistry and Physiology 29, 73–87.CrossRefGoogle Scholar
Pong, M. & Fuchs, A.F. (2000). Characteristics of the pupillary light reflex in the macaque monkey: Metrics. Journal of Neurophysiology 84, 953–963.CrossRefGoogle ScholarPubMed
Provencio, I., Jiang, G., De Grip, W.J., Hayes, W.P. & Rollag, M.D. (1998). Melanopsin: An opsin in melanophores, brain, and eye. Proceedings of the National Academy of Sciences of the United States of America 95, 340–345.CrossRefGoogle Scholar
Provencio, I., Rodriguez, I.R., Jiang, G., Hayes, W.P., Moreira, E.F. & Rollag, M.D. (2000). A novel human opsin in the inner retina. Journal of Neuroscience 20, 600–605.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1998). The First Steps in Seeing. Sunderland, MA: Sinauer Associates, Inc.Google Scholar
Schaeppi, U. & Koella, W.P. (1964). Reaction of isolated pig iris sphincter to electrical stimulation and acetylcholine. The American Journal of Physiology 206, 255–261.CrossRefGoogle ScholarPubMed
Schaeppi, U., Rubin, R. & Koella, W.P. (1966). Electrical stimulation of the isolated cat iris. The American Journal of Physiology 210, 1165–1169.CrossRefGoogle ScholarPubMed
Smith, J.D., Masek, G.A., Ichinose, L.Y., Watanabe, T. & Stark, L. (1970). Single neuron activity in the pupillary system. Brain Research 24, 219–234.CrossRefGoogle ScholarPubMed
Storey, K.B. (2007). Anoxia tolerance in turtles: Metabolic regulation and gene expression. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 147, 263–276.CrossRefGoogle Scholar
Törnqvist, G. (1970). Effect of oculomotor nerve stimulation on outflow facility and pupil diameter in a monkey (cercopithecus ethiops). Investigative Ophthalmology 9, 220–225.Google Scholar
Walls, G.L. (1942). The Vertebrate Eye and its Adaptive Radiation (1967 facsimile edition). New York: Hafner Publishing Company.Google Scholar
Warren, E.J., Allen, C.N., Brown, R.L. & Robinson, D.W. (2003). Intrinsic light responses of retinal ganglion cells projecting to the circadian system. The European Journal of Neuroscience 17, 1727–1735.CrossRefGoogle Scholar
Westheimer, G. & Blair, S.M. (1973). The parasympathetic pathways to internal eye muscles. Investigative Ophthalmology 12, 193–197.Google ScholarPubMed
Young, R.S. & Kimura, E. (2008). Pupillary correlates of light-evoked melanopsin activity in humans. Vision Research 48, 862–871.CrossRefGoogle ScholarPubMed

Dearworth supplementary material

Movie 1.mov

Download Dearworth supplementary material(Video)
Video 197.4 KB

Dearworth supplementary material

Movie 2.mov

Download Dearworth supplementary material(Video)
Video 1 MB

Dearworth supplementary material

Movie 3.mov

Download Dearworth supplementary material(Video)
Video 862.7 KB