Hostname: page-component-7c8c6479df-8mjnm Total loading time: 0 Render date: 2024-03-18T15:55:08.371Z Has data issue: false hasContentIssue false

The response dynamics of rabbit retinal ganglion cells to simulated blur

Published online by Cambridge University Press:  15 April 2010

MICHAEL L. RISNER*
Affiliation:
Department of Vision Sciences, University of Alabama at Birmingham (UAB), Birmingham, Alabama
FRANKLIN R. AMTHOR
Affiliation:
Department of Vision Sciences, University of Alabama at Birmingham (UAB), Birmingham, Alabama Department of Psychology, University of Alabama at Birmingham (UAB), Birmingham, Alabama
TIMOTHY J. GAWNE
Affiliation:
Department of Vision Sciences, University of Alabama at Birmingham (UAB), Birmingham, Alabama
*
*Address correspondence and reprint requests to: Michael L. Risner, Department of Vision Sciences, University of Alabama at Birmingham, 924 South 18th Street, Birmingham, AL 35294. E-mail: mlrisner@uab.edu

Abstract

Retinal ganglion cells (RGCs) are highly sensitive to changes in contrast, which is crucial for the detection of edges in a visual scene. However, in the natural environment, edges do not just vary in contrast, but edges also vary in the degree of blur, which can be caused by distance from the plane of fixation, motion, and shadows. Hence, blur is as much a characteristic of an edge as luminance contrast, yet its effects on the responses of RGCs are largely unexplored.

We examined the responses of rabbit RGCs to sharp edges varying by contrast and also to high-contrast edges varying by blur. The width of the blur profile ranged from 0.73 to 13.05 deg of visual angle. For most RGCs, blurring a high-contrast edge produced the same pattern of reduction of response strength and increase in latency as decreasing the contrast of a sharp edge. In support of this, we found a significant correlation between the amount of blur required to reduce the response by 50% and the size of the receptive fields, suggesting that blur may operate by reducing the range of luminance values within the receptive field. These RGCs cannot individually encode for blur, and blur could only be estimated by comparing the responses of populations of neurons with different receptive field sizes. However, some RGCs showed a different pattern of changes in latency and magnitude with changes in contrast and blur; these neurons could encode blur directly.

We also tested whether the response of a RGC to a blurred edge was linear, that is, whether the response of a neuron to a sharp edge was equal to the response to a blurred edge plus the response to the missing spatial components that were the difference between a sharp and blurred edge. Brisk-sustained cells were more linear; however, brisk-transient cells exhibited both linear and nonlinear behavior.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2010

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

Albrecht, D.G. (1995). Visual cortex neurons in monkey and cat: Effect of contrast on spatial and temporal phase transfer function. Visual Neuroscience 12, 1191–1210.CrossRefGoogle Scholar
Amthor, F.R., Keyser, K.T. & Dmitrieva, N.A. (2002). Effects of the destruction of starburst cholinergic amacrine cells by the toxin AF64A on rabbit retinal directional selectivity. Visual Neuroscience 19, 495–509.CrossRefGoogle ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989 a). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. The Journal of Comparative Neurology 280, 72–96.CrossRefGoogle ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989 b). Morphologies of rabbit retinal ganglion cells with complex receptive fields. The Journal of Comparative Neurology 280, 97–121.CrossRefGoogle ScholarPubMed
Armstrong-James, M. & Millar, J. (1979). Carbon fibre microelectrodes. Journal of Neuroscience Methods 1, 279–287.CrossRefGoogle ScholarPubMed
Barlow, H.B., Hill, R.M. & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. The Journal of Physiology 173, 377–407.Google Scholar
Bonds, A.B. (1991). Temporal dynamics of contrast gain in single cells of the cat striate cortex. Visual Neuroscience, 6, 239–255.CrossRefGoogle ScholarPubMed
Bronin, V., Mante, V. & Carandini, M. (2006). The statistical computation underlying contrast gain control. The Journal of Neuroscience 23, 6346–6353.Google Scholar
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. The Journal of Physiology 276, 257–276.Google Scholar
Carandini, M., Heeger, D.J. & Movshon, J.A. (1997). Linearity and normalization in simple cells in the macaque primary visual cortex. The Journal of Neuroscience 17, 8621–8644.CrossRefGoogle ScholarPubMed
Chander, D. & Chichilnisky, E.J. (2001). Adaptation to temporal contrast in primate and salamander retina. The Journal of Neuroscience 21, 9904–9916.CrossRefGoogle ScholarPubMed
DeVries, S.H. & Baylor, D.A. (1997). Mosaic arrangement of ganglion cell receptive fields in rabbit retina. Journal of Neurophysiology 78, 2048–2060.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Gawne, T.J. (1999). Temporal coding as a means of information transfer in the primate visual system. Critical Reviews in Neurobiology 13, 83–101.CrossRefGoogle ScholarPubMed
Gawne, T.J. (2000). The simultaneous coding of orientation and contrast in the response of V1 complex cells. Experimental Brain Research 133, 293–302.Google Scholar
Gawne, T.J., Kjaer, T.W. & Richmond, B.J. (1996). Latency: Another potential code for feature binding in striate cortex. Journal of Neurophysiology 76, 1356–1360.CrossRefGoogle ScholarPubMed
Georgeson, M.A. & Sullivan, G.D. (1975). Contrast contstancy: Deblurring in human vision by spatial frequency channels. The Journal of Physiology 252, 627–656.CrossRefGoogle ScholarPubMed
Hamerly, J.R. & Dvorak, C.A. (1981). Dectection and discrimination of blur in edges and lines. Journal of the Optical Society of America 71, 448–452.CrossRefGoogle Scholar
Hughes, A. (1971). Topographical relationship between the anatomy and physiology of the rabbit visual system. Documenta Ophthalmologica 30, 33–159.Google Scholar
Hughes, A. (1972). A schematic eye for the rabbit. Vision Research 12, 123–138.Google Scholar
Ikeda, H. & Hill, R.M. (1971). Can a peripheral retinal ganglion cell respond differentially to images in or out of focus? Nature 229, 557–558.CrossRefGoogle ScholarPubMed
Koch, K., McLean, J., Segev, R., Freed, M.A., Berry, M.J. II, Balasubramanian, V. & Sterling, P. (2006). How much the eye tells the brain. Current Biology 16, 1428–1434.Google Scholar
Lee, J.M. & Hill, R.M. (1972). Sensitivity of the midbrain to blur. American Journal of Optometry 49, 709–712.CrossRefGoogle ScholarPubMed
Lee, J., Williford, T. & Maunsell, J.H. (2007). Spatial attention and the latency and the neuronal responses in macaque area V4. The Journal of Neuroscience 27, 9632–9637.CrossRefGoogle ScholarPubMed
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit’s retina. The Journal of Physiology 188, 285–307.CrossRefGoogle Scholar
Levick, W.R. (1973). Variations in the response latency of cat retinal ganglion cells. Vision Research 13, 837–853.Google Scholar
Levine, M.W. & Cleland, B.G. (2001). An analysis of the effect of retinal ganglion cell impulses upon the firing probability of neurons in the dorsal lateral geniculate nucleus. Brain Research 902, 244–254.CrossRefGoogle ScholarPubMed
Marc, R.E. & Jones, B.W. (2002). Molecular phenotyping of retinal ganglion cells. The Journal of Neuroscience 22, 413–427.CrossRefGoogle ScholarPubMed
Marmor, M.F. & Gawande, A. (1988). Effect of visual blur on contrast sensitivity. Clinical implications. Ophthalmology 95, 139–143.CrossRefGoogle ScholarPubMed
Mather, G. & Smith, D.R.R. (2000). Depth cue integration: Stereopsis and image blur. Vision Research 40, 3501–3506.CrossRefGoogle ScholarPubMed
Ohzawa, I. Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat’s visual system. Journal of Neurophysiology, 54, 651–667.CrossRefGoogle ScholarPubMed
Pentland, A.P. (1987). A new sense for depth of field. IEEE Transactions on Pattern Analysis and Machine Intelligence 9, 523–31.CrossRefGoogle ScholarPubMed
Powers, M.K. & Green, D.G. (1978). Single retinal ganglion cell responses in the dark-reared rat: Grating acuity, contrast sensitivity, and defocusing. Vision Research, 18, 1533–1539.CrossRefGoogle ScholarPubMed
Reid, R.C., Victor, J.D. & Shapley, R.M. (1992). Broadband temporal stimuli decrease the integration time of neurons in cat striate cortex. Visual Neuroscience 9, 39–45.CrossRefGoogle ScholarPubMed
Renna, J.M., Strang, C.E., Amthor, F.R. & Keyser, K.T. (2007). Strychnine, but not PMBA, inhibits neuronal nicotine acetylcholine receptors expressed by rabbit retinal ganglion cells. Visual Neuroscience 24, 503–511.Google Scholar
Risner, M.L. & Gawne, T.J. (2009). Response dynamics of primate early visual cortical neurons to simulated optical blur. Visual Neuroscience 26, 411–420.CrossRefGoogle Scholar
Risner, M.L., Nowak, P., Amthor, F.R. & Gawne, T.J. (2009). Response dynamics of retinal ganglion cells to simulated blur. Society for Neuroscience Abstract 165.18.Google Scholar
Sclar, G. & Freeman, R.D. (1982). Orientation selectivity in the cat’s striate cortex is invariant with stimulus contrast. Experimental Brain Research 46, 457–461.CrossRefGoogle ScholarPubMed
Sestokas, A.K., Lehmkuhle, S. & Kratz, K.E. (1991). Relationship between response latency and amplitude forganglion and geniculate X- and Y-cells in the cat. The International Journal of Neuroscience 60, 59–64.CrossRefGoogle ScholarPubMed
Shapley, R. & Lennie, P. (1985). Spatial frequency analysis in the visual system. Annual Review of Neuroscience 8, 547–581.CrossRefGoogle ScholarPubMed
Shapley, R. & Victor, J.D. (1978). The effect of contrast on the transfer properties of cat retinal ganglion cells. The Journal of Physiology 285, 275–298.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Victor, J.D. (1979). Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. The Journal of Physiology 290, 141–61.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Victor, J.D. (1980). The effect of contrast on the non-linear response of the Y cell. The Journal of Physiology 302, 535–547.Google Scholar
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. The Journal of Physiology 318, 161–179.CrossRefGoogle ScholarPubMed
Siguenza, J., Heide, W. & Creutzfeldt, O.D. (1987). Representation of edges of variable blur by neuronal responses in the lateral geniculate body and the visual cortex of cats: Limits of linear prediction. Vision Research 27, 1701–1717.Google Scholar
Sinich, L.C., Adams, D.L., Economides, J.R. & Horton, J.C. (2007). Transmission of spike trains at the retinogeniculate synapse. The Journal of Neuroscience 45, 107–120.Google Scholar
Usrey, W.M., Reppas, J.B. & Reid, R.C. (1998). Paired-spike interactions and synaptic efficacy of retinal input to thalamus. Nature 395, 384–387.Google Scholar
van Hof, M.W. (1967). Visual acuity in the rabbit. Vision Research 7, 749–751.Google Scholar
van Wyk, M., Taylor, W.R. & Vaney, D.I. (2006). Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina. The Journal of Neuroscience 26, 13250–13263.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1980). The grating acuity of the wild European rabbit. Vision Research 20, 87–89.CrossRefGoogle ScholarPubMed
Vaney, D.I., Levick, W.R. & Thibos, L.N. (1981). Rabbit retinal ganglion cells. Experimental Brain Research 44, 27–33.CrossRefGoogle ScholarPubMed
Wang, B. & Ciuffreda, K.J. (2005 a). Foveal blur discrimination of the human eye. Ophthalmic & Physiological Optics 25, 45–511.CrossRefGoogle ScholarPubMed
Wang, B. & Ciuffreda, K.J. (2005 b). Blur discrimination of the human eye in the near retinal periphery. Optometry and Vision Sciences 82, 52–58.Google Scholar
Watt, R.J. & Morgan, M.J. (1983). The recognition and representation of edge blur: Evidence for spatial primitives in human vision. Vision Research 23, 1465–1477.Google Scholar
Westheimer, G., Brincat, S. & Wehrhahn, C. (1999). Contrast dependency of foveal spatial functions: Orientation, vernier, separation, blur, and displacement discrimination and the tilt Poggendorff illusions. Vision Research 39, 1631–1639.CrossRefGoogle ScholarPubMed
Zaghloul, K.A., Boahen, K. & Demb, J.B. (2005). Contrast adaptation in subthreshold and spiking responses of mammalian Y-type retinal ganglion cells. The Journal of Neuroscience 23, 860–868.Google Scholar
Zeck, G.M. & Masland, R.H. (2007). Spike train signatures of retinal ganglion cell types. The European Journal of Neuroscience 26, 367–380.CrossRefGoogle ScholarPubMed
Zeck, G.M., Xiao, Q. & Masland, R.H. (2005). The spatial filtering properties of local edge detectors and brisk-sustained retinal ganglion cells. The European Journal of Neuroscience 22, 2016–2026.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Risner supplementary material

Figure S1.tif

Download Risner supplementary material(Image)
Image 662.1 KB
Supplementary material: Image

Risner supplementary material

Figure S2.tif

Download Risner supplementary material(Image)
Image 653.6 KB
Supplementary material: Image

Risner supplementary material

Figure S3.tif

Download Risner supplementary material(Image)
Image 826.9 KB
Supplementary material: Image

Risner supplementary material

Figure S4.tif

Download Risner supplementary material(Image)
Image 687.8 KB
Supplementary material: Image

Risner supplementary material

Figure S5.tif

Download Risner supplementary material(Image)
Image 830.8 KB
Supplementary material: Image

Risner supplementary material

Figure S6.tif

Download Risner supplementary material(Image)
Image 1.1 MB