Hostname: page-component-848d4c4894-xfwgj Total loading time: 0 Render date: 2024-06-27T11:12:32.786Z Has data issue: false hasContentIssue false

Responses of the teleostean nucleus isthmi to looming objects and other moving stimuli

Published online by Cambridge University Press:  24 April 2006

SHAWN P. GALLAGHER
Affiliation:
Department of Psychology, Millersville University, Milersville, Pennsylvania
DAVID P.M. NORTHMORE
Affiliation:
Department of Psychology, University of Delaware, Newark, Delaware

Abstract

Visually evoked extracellular neural activity was recorded from the nucleus isthmi (NI) of goldfish and bluegill sunfish. When moving anywhere within the right eye's visual field, three-dimensional checkered balls or patterns on a computer screen evoked bursts of spikes in the left NI. Object motion parallel to the longitudinal body axis gave responses that habituated markedly upon repetition, but movement into recently unstimulated regions of the visual field gave vigorous responses. Thus, while NI's response is not visuotopic, its habituation is. An object approaching the animal's body generated a rising spike density, whereas object recession generated only a transient burst. During the approach of a checkered stimulus ball, average NI spike density rose linearly as the ball-to-eye distance decreased and at a rate proportional to the ball's speed (2.5–30 cm/s). Increasing ball size (2.2–9.2 cm) did not affect the rate of activity rise at a given speed, but did increase overall activity levels. NI also responded reliably to expanding textures of fixed overall size. The results suggest that NI signals changes in motion of objects relative to the fish, and estimates the proximity of approaching objects.

Type
Research Article
Copyright
2006 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

Brandis, A. & Saidel, W.M. (2001). Nucleus isthmi: The modulator of binocular vision in fish. Bulletin of the New Jersey Academy of Sciences 46, 22.Google Scholar
Collett, T.S., Udin, S.B., & Finch, D.J. (1987). A possible mechanism for binocular depth judgments in anurans. Experimental Brain Research 66, 3540.Google Scholar
Cui, H. & Malpeli, J.G. (2003). Activity in the parabigeminal nucleus during eye movements directed at moving and stationary targets. Journal of Neurophysiology 89, 31283142.CrossRefGoogle Scholar
Dunn-Meynell, A.A. & Sharma, S.C. (1984). Changes in the topographically organized connections between the nucleus isthmi and the optic tectum after partial tectal ablation in adult goldfish. Journal of Comparative Neurology 227, 497510.CrossRefGoogle Scholar
Glasser, S. & Ingle, D. (1978). The nucleus isthmus as a relay station in the ipsilateral visual projection to the frog's optic tectum. Brain Research 159, 214218.CrossRefGoogle Scholar
Graybiel, A.M. (1978). A satellite system of the superior colliculus: The parabigeminal nucleus and its projections to the superficial collicular layers. Brain Research 145, 365374.CrossRefGoogle Scholar
Grobstein, P. & Cromer, C. (1983). The nucleus isthmi as an intertectal relay for the ipsilateral oculotectal projection in the frog, Rana pipiens. Journal of Comparative Neurology 217, 5474.CrossRefGoogle Scholar
Grobstein, P., Cromer, C., Hollyday, M., & Archer, S.M. (1978). A crossed isthmo-tectal projection in Rana pipiens and its involvement in the ipsilateral visuotectal projection. Brain Research 156, 11723.CrossRefGoogle Scholar
Grover, B.G. & Sharma, S.C. (1981). Organization of extrinsic tectal connections in goldfish (Carassius auratus). Journal of Comparative Neurology 196, 471488.CrossRefGoogle Scholar
Gruberg, E.R. (1983). Recent work on the nucleus isthmi and its niche in the visual system. In Progress in Nonmammalian Brain Research, Vol. I, ed. Nistico, G. & Bolis, L., pp. 159174. Boca Raton, Florida: CRC Press.
Gruberg, E.R. & Udin, S.B. (1978). Topographic projections between the nucleus isthmi and the tectum of the frog Rana pipiens. Journal of Comparative Neurology 179, 487500.CrossRefGoogle Scholar
Gruberg, E.R., Wallace, M.T., Caine, H.S., & Mote, M.I. (1991). Behavioral and physiological consequences of unilateral ablation of the nucleus isthmi in the leopard frog. Brain, Behavior, and Evolution 37, 92103.Google Scholar
Guthrie, D.M. & Banks, J.R. (1978). The receptive field structure of visual cells from the optic tectum of the freshwater perch (Perca fluviatilis). Brain Research 141, 211225.CrossRefGoogle Scholar
Ito, H., Sakamoto, N., & Takatsuji, K. (1982). Cytoarchitecture, fiber connections, and ultrastructure of nucleus isthmi in a teleost (Navodon modestus) with a special reference to degenerating isthmic afferents from optic tectum and nucleus pretectalis. Journal of Comparative Neurology 205, 299311.CrossRefGoogle Scholar
Judge, S.J. & Rind, F.C. (1997). The locust DCMD, a movement detecting neurone tightly tuned to collision trajectories. Journal of Experimental Biology 200, 22092216.Google Scholar
Kawasaki, M. & Aoki, K. (1983). Visual responses recorded from the optic tectum of Japanese dace, Tribolodon halonensis. Journal of Comparative Physiology A 152, 147153.CrossRefGoogle Scholar
King, W.M. & Schmidt, J.T. (1993). Nucleus isthmi in goldfish: In vitro recordings and fiber connections revealed by HRP injections. Visual Neuroscience 10, 419437.CrossRefGoogle Scholar
Meek, J. (1983). Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum. Brain Research Reviews 6, 247297.Google Scholar
Northmore, D.P.M. (1989). Quantitative electrophysiological studies of regenerating visuotopic maps in goldfish. I. Early recovery of dimming sensitivity in tectum and torus longitudinalis. Neuroscience 32, 739747.Google Scholar
Northmore, D.P.M. (1991). Visual responses of nucleus isthmi in a teleost fish (Lepomis macrochirus). Vision Research 31, 525535.CrossRefGoogle Scholar
Northmore, D.P.M. & Gallagher, S.P. (2003). Functional relationship between nucleus isthmi and tectum in teleosts: Synchrony but no topography. Visual Neuroscience 20, 335348.CrossRefGoogle Scholar
O'Benar, J.D. (1976). Electrophysiology of neural units in goldfish optic tectum. Brain Research Bulletin 1, 529541.CrossRefGoogle Scholar
O'Shea, M. & Williams, J.L.D. (1974). The anatomy and output connection of a locust visual interneurone: The lobular giant movement detector (LGMD) neurone. Journal of Comparative Physiology 91, 257266.CrossRefGoogle Scholar
Pérez-Pérez, M.P., Luque, M.A., Herrero, L., Núñez-Abades, P.A., & Torres, B. (2003). Afferent connectivity to different functional zones of the optic tectum of goldfish. Visual Neuroscience 20, 397410.CrossRefGoogle Scholar
Rind, F.C & Bramwell, D.I. (1996). Neural network based on the input organization of an identified neuron signaling impending collision. Journal of Neurophysiology 75, 967985.Google Scholar
Rowell, C.H.F., O'Shea, M., & Williams, J.L.D. (1977). The neuronal basis of a sensory analyser, the acridid movement detector system. Journal of Experimental Biology 68, 157185.Google Scholar
Sakamoto, N., Ito, H., & Udea, S. (1981). Topographic projections between the nucleus isthmi and the optic tectum in a teleost, Navodon modestus. Brain Research 224, 225234.CrossRefGoogle Scholar
Schlotterer, G.R. (1977). Response of the locust descending contralateral movement detector to rapidly approaching and withdrawing visual stimuli. Canadian Journal of Zoology 55, 13721376.CrossRefGoogle Scholar
Sereno, M.I. & Ulinski, P.S. (1987). Caudal topographic nucleus isthmi and the rostral nontopographic nucleus isthmi in the turtle, Pseudemys scripta. Journal of Comparative Neurology 261, 319346.CrossRefGoogle Scholar
Sun, H. & Frost, B.J. (1998). Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nature Neuroscience 1, 296303.Google Scholar
Vanegas, H. & Ito, H. (1983). Morphological aspects of the teleostean visual system: A review. Brain Research Review 6, 117137.CrossRefGoogle Scholar
Wang, S.-R. (2003). The nucleus isthmi and dual modulation of the receptive field of tectal neurons in non-mammals. Brain Research Review 41, 1325.CrossRefGoogle Scholar
Wang, Y.C. & Frost, B.J. (1991). Visual response characteristics of neurons in the nucleus isthmi magnocellularis and nucleus isthmi parvocellularis of pigeons. Experimental Brain Research 87, 624633.Google Scholar
Wiggers, W. & Roth, G. (1991). Anatomy, neurophysiology and functional aspects of the nucleus isthmi in salamanders of the family Plethodontidae. Journal of Comparative Physiology A 169, 165176.CrossRefGoogle Scholar
Williams, B., Hernandez, N., & Vanegas, H. (1983). Electrophysiological analysis of the teleostean nucleus isthmi and its relationship with the optic tectum. Journal of Comparative Physiology A 152, 545554.CrossRefGoogle Scholar
Xue, H.-G., Yamamoto, N., Yoshimoto, M., Yang, C.-Y., & Ito, H. (2001). Fiber connections of the nucleus isthmi in the carp (Cyprinis carpio) and Tilapia (Oreochromis niloticus). Brain, Behavior, and Evolution 58, 185204.Google Scholar