Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-19T16:37:46.357Z Has data issue: false hasContentIssue false
  • English
  • Français

Center/surround organization of retinal bipolar cells: High correlation of fundamental responses of center and surround to sinusoidal contrasts

Published online by Cambridge University Press:  25 March 2011

DWIGHT A. BURKHARDT ,
THEODORE M. BARTOLETTI  and
WALLACE B. THORESON
DWIGHT A. BURKHARDT*
Affiliation:
Department of Psychology and Graduate Program in Neuroscience, University of Minnesota, Minneapolis, Minnesota
THEODORE M. BARTOLETTI
Affiliation:
Departments of Ophthalmology & Visual Science and Pharmacology & Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska
WALLACE B. THORESON
Affiliation:
Departments of Ophthalmology & Visual Science and Pharmacology & Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska
*
*Address correspondence and reprint requests to: Dwight A. Burkhardt, Department of Psychology, n218 Elliott Hall, University of Minnesota, 75 East River Road, Minneapolis, MN 55455. E-mail: burkh001@umn.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Receptive field organization of cone-driven bipolar cells was investigated by intracellular recording in the intact light-adapted retina of the tiger salamander (Ambystoma tigrinum). Centered spots and concentric annuli of optimum dimensions were used to selectively stimulate the receptive field center and surround with sinusoidal modulations of contrast at 3 Hz. At low contrasts, responses of both the center and surround of both ON and OFF bipolar cells were linear, showing high gain and thus contrast enhancement relative to cones. The contrast/response curves for the fundamental response, measured by a Fast Fourier Transform, reached half maximum amplitude quickly at 13% contrast followed by saturation at high contrasts. The variation of the normalized amplitude of the center and surround responses was remarkably similar, showing linear regression over the entire response range with very high correlations, r2 = 0.97 for both ON and OFF cells. The contrast/response curves of both center and surround for both ON and OFF cells were well fit (r2 = 0.98) by an equation for single-site binding. In about half the cells studied, the nonlinear waveforms of center and surround could be brought into coincidence by scaling and shifting the surround response in time. This implies that a nonlinearity, common to both center and surround, occurs after polarity inversion at the cone feedback synapse. Evidence from paired whole-cell recordings between single cones and OFF bipolar cells suggests that substantial nonlinearity is not due to transmission at the cone synapse but instead arises from intrinsic bipolar cell and network mechanisms. When sinusoidal contrast modulations were applied to the center and surround simultaneously, clear additivity was observed for small responses in both ON and OFF cells, whereas the interaction was strikingly nonadditive for large responses. The contribution of the surround was then greatly reduced, suggesting attenuation at the cone feedback synapse.

Keywords

Retinal bipolar cellsCenter/surround receptive fieldContrast responses
Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 3 , May 2011 , pp. 183 - 192
Copyright
Copyright © Cambridge University Press 2011

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

Awatramani, G. & Slaughter, M.M. (2000). Origin of transient and sustained responses in ganglion cells of the retina. The Journal of Neuroscience 15, 7087–7095.Google Scholar
Baccus, S.A. & Meister, M. (2002). Fast and slow contrast adaptation in retinal circuitry. Neuron 36, 909–919.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. (1974). Sensitization and center-surround antagonism in Necturus retina. The Journal of Physiology 236, 593–610.Google Scholar
Burkhardt, D.A. (2010). Contrast processing by ON and OFF bipolar cells. Visual Neuroscience 28, 69–75.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. & Fahey, P.K. (1998). Contrast enhancement and distributed encoding by bipolar cells in the retina. Journal of Neurophysiology 80, 1070–1081.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Fahey, P.K. & Sikora, M.A. (2004). Retinal bipolar cells: Contrast encoding for sinusoidal modulation and steps of luminance contrast. Visual Neuroscience 21, 883–893.Google Scholar
Cadetti, L., Tranchina, D. & Thoreson, W.B. (2005). A comparison of release kinetics and glutamate receptor properties in shaping rod-cone differences in EPSP kinetics in the salamander retina. Journal of Physiology (London) 569, 773–788.Google Scholar
Cadetti, L. & Thoreson, W.B. (2006). Feedback effects of horizontal cell membrane potential on cone calcium currents studied with simultaneous recordings. Journal of Neurophysiology 95, 1992–1995.CrossRefGoogle ScholarPubMed
Dacey, D., Packer, O.S., Diller, L., Brainard, D., Peterson, B. & Lee, B. (2000). Center surround receptive field structure of cone bipolar cells in primate retina. Vision Research 40, 1801–1811.Google Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, MA: Belknap Press.Google Scholar
Fahey, P.K. & Burkhardt, D.A. (2001). Effects of light adaptation on contrast processing in bipolar cells in the retina. Visual Neuroscience 18, 581–597.Google Scholar
Fahey, P.K. & Burkhardt, D.A. (2003). Center-surround organization in bipolar cells: Symmetry for opposing contrasts. Visual Neuroscience 20, 1–10.Google Scholar
Hare, W.A., Lowe, J.S. & Owen, G. (1986). Morphology of physiologically identified bipolar cells in the retina of the tiger salamander, Ambystoma tigrinum. The Journal of Comparative Neurology 252, 130–138.CrossRefGoogle ScholarPubMed
Hare, W.A. & Owen, W.G. (1990). Spatial organization of the bipolar cell’s receptive field in the retina of the tiger salamander. The Journal of Physiology 421, 223–245.Google Scholar
Hare, W.A. & Owen, W.G. (1996). Receptive field of the retinal bipolar cell: A pharmacological study in the tiger salamander. Journal of Neurophysiology 76, 2005–2019.CrossRefGoogle ScholarPubMed
Hirasawa, H. & Kaneko, A. (2003). pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. The Journal of General Physiology 122, 657–671.CrossRefGoogle ScholarPubMed
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37–68.Google Scholar
Miller, R.F. (2008). Cell communication mechanisms in the vertebrate retina. Investigative Ophthalmology & Visual Science 49, 5184–5198.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (2004). ON and OFF pathways in the vertebrate retina and visual system. In The Visual Neurosciences, Vol. 1, ed. Chalupa, L.M. & Werner, J.S., pp. 260–278. Cambridge, MA: MIT Press.Google Scholar
Packer, S., Verweij, J., Li, P., Schnapf, J.L. & Dacey, D.M. (2010). Blue- yellow opponency in primate S cone photoreceptors. The Journal of Neuroscience 30, 568–572.CrossRefGoogle ScholarPubMed
Rieke, F. (2001). Temporal contrast adaptation in salamander bipolar cells. The Journal of Neuroscience 21, 9445–9454.Google Scholar
Sterling, P. (2004). How retinal circuits optimize the transfer of visual information. In The Visual Neurosciences, Vol. 1, ed. Chalupa, L.M. & Werner, J.S., pp. 234–259. Cambridge, MA: MIT Press.Google Scholar
Thoreson, W.B. & Miller, R.F. (1996). Removal of intracellular chloride suppresses transmitter release from photoreceptor terminals. The Journal of General Physiology 107, 631–642.CrossRefGoogle Scholar
Werblin, F.S. & Dowling, J.E. (1968). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339–355.Google Scholar
Witkovsky, P. & Stone, S. (1987). Center-surround organization and its modification by gamma-aminobutyric acid and strontium. Experimental Biology 1, 1–12.Google Scholar
Wu, S.M. (2010). Synaptic organization of the vertebrate retina: General principles and species-specific variations. Investigative Ophthalmology & Visual Science 51, 1264–1274.Google Scholar
Wu, S.M., Gao, F. & Maple, B.R. (2000). Functional architecture of synapses in the inner retina: Segregation of visual signals by stratification of bipolar cell axon terminals. The Journal of Neuroscience 20, 4462–4470.CrossRefGoogle ScholarPubMed
Wunk, D.F. & Werblin, F.S. (1979). Synaptic inputs to ganglion cells in the tiger salamander retina. The Journal of General Physiology 73, 265–286.CrossRefGoogle ScholarPubMed
Zhang, A.J. & Wu, S.M. (2009). Receptive fields of retinal bipolar cells are mediated by heterogeneous synaptic activity. The Journal of Neuroscience 29, 787–797.Google Scholar