Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-26T02:08:58.707Z Has data issue: false hasContentIssue false
  • English
  • Français

Evidence for local circuits within the receptive fields of retinal ganglion cells in goldfish

Published online by Cambridge University Press:  02 June 2009

Michael W. Levine  and
Roger P. Zimmerman
Michael W. Levine
Affiliation:
The University of Illinois at Chicago, Department of Psychology and the Committee on Neuroscience, Chicago
Roger P. Zimmerman
Affiliation:
Departments of Neurological Sciences and Physiology, Rush Medical College, Chicago
Get access Rights & Permissions [Opens in a new window]

Abstract

A new form of receptive field map, the response-component map, was developed to identify points within a receptive field that produce similar response patterns. The fields were probed with discretely flashed small spots of light. The magnitudes of the responses to stimulus onset and to stimulus offset elicited at each point were represented on the map by a vector radiating from the position representing the location of that point. Thus, response-component maps preserve the spatial distributions of responsivity and temporal nonlinearities. Points with similar response patterns were identified from a scatterplot in which the response at each spatial position was located in a plane representing the angles of the response-component vectors. Points with similar response characteristics that were also spatially contiguous were considered as a distinct response subregion within the receptive field.

Barely 10% of the receptive fields of goldfish ganglion cells mapped with this technique proved as simple as the traditional concentric field described for retinal cells. In at least 17% of the cases, the field showed three concentric rings, with a very small “inner center” within the center of the field. In at least 50% of the cases, response subregions of different type lay side by side, rather than in a concentric configuration. Some subregions could be differentiated by the relative strengths of the responses to onset and offset of the stimulus spot, supporting the hypothesis that a push-pull system generates ganglion cell responses. Subregions were evident in successive mappings of the same cell, demonstrating they are not due to the vagaries of individual responses. They probably represent the spatial domains (or their intersections) of individual interneurons distal to the retinal ganglion cells. It is possible that position within the receptive field may be coded by the temporal pattern of the responses.

Keywords

Retinal ganglion cellsGoldfish retinaReceptive fields
Type
Research Articles
Information
Visual Neuroscience , Volume 1 , Issue 4 , July 1988 , pp. 377 - 385
Copyright
Copyright © Cambridge University Press 1988

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

Bilotta, J. & Abramov, I. (1985). Spatial properties of goldfish ganglion cells. Investigative Ophthalmology and Visual Science (Suppl.) 26, 117.Google Scholar
Cazalis, M., Dayanithi, G. & Nordmann, J. J. (1985). The role of patterned burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe. Journal of Physiology 369, 45–60.Google Scholar
Chung, S.H., Raymond, S. A. & Lettvin, J. Y. (1970). Multiple meaning in single visual units. Brain, Behavior, and Evolution 3, 72–101.Google Scholar
Cleland, B. C, Levick, W. R. & Sanderson, K. J. (1973). Properties of sustained and transient ganglion cells in the cat retina. Journal of Physiology 228, 649–680.Google Scholar
Davis, G. W. & Naka, K.I. (1980). Spatial organizations of catfish retinal neurons. 1. Single and random-bar stimulation. Journal of Neurophysiology 43, 807–831.Google Scholar
Daw, N. W. (1967). Goldfish retina: organization for simultaneous color contrast. Science (NY) 158, 942–944.CrossRefGoogle ScholarPubMed
Daw, N. W. (1968). Colour-coded ganglion cells in the goldfish retina: extension of their receptive fields by means of new stimuli. Journal of Physiology 197, 567–592.Google Scholar
Enroth-Cugell, C. & FReeman, A. W. (1987). The receptive field spatial structure of cat retinal Y cells. Journal of Physiology 384, 49–79.Google Scholar
Enroth-Cugell, C. & Robson, J. G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C, Robson, J. G., Schweitzer-Tong, D. E. & Watson, A. B. (1983). Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation. Journal of Physiology 341, 279–307.CrossRefGoogle ScholarPubMed
Gordon, J. & Shapley, R. M. (1978). Contrast sensitivity and spatial summation in frog and eel retinal ganglion cells. In Visual Psychophysics and Physiology, ed. Armington, J. C, Krauskopf, J. & Wooten, B. R., pp. 315–329. New York: Academic Press.CrossRefGoogle Scholar
Hochstein, S. & Shapley, R. M. (1976). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology 262, 265–284.Google Scholar
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar, and amacrine cells in goldfish retina. Journal of Physiology 207, 623–633.Google Scholar
Kaneko, A. (1973). Receptive field organization of bipolar and amacrine cells in the goldfish retina. Journal of Physiology 235, 133–153.Google Scholar
Kuffler, S. W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37–68.CrossRefGoogle ScholarPubMed
Lasater, E. M. (1982). Spatial receptive fields of catfish retinal ganglion cells. Journal of Neurophysiology 48, 823–835.CrossRefGoogle ScholarPubMed
Levine, M. W. & Shefner, J. M. (1977). Variability in ganglion cell firing patterns; implications for separate “on” and “off” processes. Vision Research 17, 765–776.CrossRefGoogle Scholar
Levine, M. W. & Shefner, J. M. (1979). X-like and not-X-like cells in goldfish retina. Vision Research 19, 95–97.Google Scholar
Levine, M. W. & Shefner, J. M. (1981). Distance-dependent interactions between the rod and the cone systems in goldfish retina. Experimental Brain Research 44, 353–361.Google Scholar
Levine, M. W. & Zimmerman, R. P. (1985). Mechanisms contributing to the receptive fields of ganglion cells in the retinae of fish. Investigative Ophthalmology and Visual Science (Suppl.) 26, 263.Google Scholar
Macy, A. & Easter, S. S., JR. (1981). Growth-related changes in the size of receptive field centers of retinal ganglion cells in goldfish. Vision Research 21, 1497–1504.Google Scholar
McGuire, B. A., Stevens, J. K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. Journal of Neuroscience 6, 907–918.Google Scholar
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Rodieck, R. W. & Stone, J. (1965). Analysis of receptive fields of cat retinal ganglion cells. Journal of Neurophysiology 28, 833–849.Google Scholar
Shapley, R., Dawis, S. & Kaplan, E. (1985). The receptive field surround's temporal response properties are spatially inhomogeneous. Investigative Ophthalmology and Visual Science (Suppl.) 26, 195.Google Scholar
Shapley, R. M. & Gordon, J. (1978). The eel retina: ganglion cell classes and spatial mechanisms. Journal of General Physiology 71, 138–155.Google ScholarPubMed
Shefner, J. M. & Levine, M. W. (1979). A comparison of properties of goldfish retinal ganglion cells as a function of lighting conditions during dissection. Vision Research 19, 83–89.Google Scholar
Soodak, R. E., Shapley, R. M. & Kaplan, E. (1987). Functional subunits of receptive field centers in cat X and Y cells. Investigative Ophthalmology and Visual Science (Suppl.) 28, 240.Google Scholar
Spekreijse, H., Wagner, H. G. & Wolbarsht, M. L. (1972). Spectral and spatial coding of ganglion cell responses in goldfish retina. Journal of Neurophysiology 35, 73–86.Google Scholar
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.Google Scholar
Thibos, L. N. & Levick, W. R. (1983). Bimodal receptive fields of cat retinal ganglion cells. Vision Research 23, 1561–1572.Google Scholar