Ganglion Cell Adaptability: Does the Coupling of Horizontal Cells Play a Role?

Background The visual system can adjust itself to different visual environments. One of the most well known examples of this is the shift in spatial tuning that occurs in retinal ganglion cells with the change from night to day vision. This shift is thought to be produced by a change in the ganglion cell receptive field surround, mediated by a decrease in the coupling of horizontal cells. Methodology/Principal Findings To test this hypothesis, we used a transgenic mouse line, a connexin57-deficient line, in which horizontal cell coupling was abolished. Measurements, both at the ganglion cell level and the level of behavioral performance, showed no differences between wild-type retinas and retinas with decoupled horizontal cells from connexin57-deficient mice. Conclusion/Significance This analysis showed that the coupling and uncoupling of horizontal cells does not play a dominant role in spatial tuning and its adjustability to night and day light conditions. Instead, our data suggest that another mechanism, likely arising in the inner retina, must be responsible.

[1]  J. H. van Hateren,et al.  A theory of maximizing sensory information , 2004, Biological Cybernetics.

[2]  A. Ball,et al.  Background illumination reduces horizontal cell receptive-field size in both normal and 6-hydroxydopamine-lesioned goldfish retinas , 1991, Visual Neuroscience.

[3]  R. W. Rodieck,et al.  Analysis of receptive fields of cat retinal ganglion cells. , 1965, Journal of neurophysiology.

[4]  P. Witkovsky,et al.  Sub-millimolar cobalt selectively inhibits the receptive field surround of retinal neurons , 1999, Visual Neuroscience.

[5]  D. Dacey,et al.  The Classical Receptive Field Surround of Primate Parasol Ganglion Cells Is Mediated Primarily by a Non-GABAergic Pathway , 2004, The Journal of Neuroscience.

[6]  C Blakemore,et al.  On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images , 1969, The Journal of physiology.

[7]  E. Pugh,et al.  UV- and Midwave-Sensitive Cone-Driven Retinal Responses of the Mouse: A Possible Phenotype for Coexpression of Cone Photopigments , 1999, The Journal of Neuroscience.

[8]  S. Nawy,et al.  The gap junction blockers carbenoxolone and 18β-glycyrrhetinic acid antagonize cone-driven light responses in the mouse retina , 2003, Visual Neuroscience.

[9]  K I Naka,et al.  Dogfish ganglion cell discharge resulting from extrinsic polarization of the horizontal cells , 1972, The Journal of physiology.

[10]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[11]  J. Robson,et al.  The Scotopic Threshold Response of the Dark‐Adapted Electroretinogram of the Mouse , 2002, The Journal of physiology.

[12]  R. Jensen,et al.  Effects of dopamine antagonists on receptive fields of brisk cells and directionally selective cells in the rabbit retina , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  H. Barlow Summation and inhibition in the frog's retina , 1953, The Journal of physiology.

[14]  C. Enroth-Cugell,et al.  Adaptation and dynamics of cat retinal ganglion cells , 1973, The Journal of physiology.

[15]  S. Nirenberg,et al.  Selective Ablation of a Class of Amacrine Cells Alters Spatial Processing in the Retina , 2004, The Journal of Neuroscience.

[16]  Joseph J. Atick,et al.  What Does the Retina Know about Natural Scenes? , 1992, Neural Computation.

[17]  Yu Wang,et al.  A circadian clock regulates rod and cone input to fish retinal cone horizontal cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Yumiko Umino,et al.  Speed, Spatial, and Temporal Tuning of Rod and Cone Vision in Mouse , 2008, The Journal of Neuroscience.

[19]  S. Mangel,et al.  Analysis of the horizontal cell contribution to the receptive field surround of ganglion cells in the rabbit retina. , 1991, The Journal of physiology.

[20]  C. Enroth-Cugell,et al.  Spatio‐temporal interactions in cat retinal ganglion cells showing linear spatial summation. , 1983, The Journal of physiology.

[21]  Timm Schubert,et al.  Horizontal cell receptive fields are reduced in connexin57‐deficient mice , 2006, The European journal of neuroscience.

[22]  R. Weiler,et al.  Endogenous dopaminergic regulation of horizontal cell coupling in the mammalian retina , 2000, The Journal of comparative neurology.

[23]  K. Yau,et al.  Diminished Pupillary Light Reflex at High Irradiances in Melanopsin-Knockout Mice , 2003, Science.

[24]  S. Bloomfield,et al.  Dark‐ and light‐induced changes in coupling between horizontal cells in mammalian retina , 1999, The Journal of comparative neurology.

[25]  R. Weiler,et al.  Protein Kinase A-mediated Phosphorylation of Connexin36 in Mouse Retina Results in Decreased Gap Junctional Communication between AII Amacrine Cells* , 2006, Journal of Biological Chemistry.

[26]  D. Copenhagen,et al.  Sodium action potentials are not required for light-evoked release of GABA or glycine from retinal amacrine cells. , 1999, Journal of neurophysiology.

[27]  D. A. Burkhardt,et al.  Center-surround organization in bipolar cells: Symmetry for opposing contrasts , 2003, Visual Neuroscience.

[28]  W R Taylor,et al.  TTX attenuates surround inhibition in rabbit retinal ganglion cells , 1999, Visual Neuroscience.

[29]  P. Cook,et al.  Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells , 1998, Nature Neuroscience.

[30]  Picaud Serge,et al.  The optomotor response: A robust first-line visual screening method for mice , 2005, Vision Research.

[31]  R A Smith,et al.  Luminance‐dependent changes in mesopic visual contrast sensitivity , 1973, The Journal of physiology.

[32]  Mark W. Greenlee,et al.  The time course of adaptation to spatial contrast , 1991, Vision Research.

[33]  J. Dowling,et al.  Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. , 1969, Journal of neurophysiology.

[34]  P. O. Bishop,et al.  Spatial vision. , 1971, Annual review of psychology.

[35]  A. Kaneko Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina , 1970, The Journal of physiology.

[36]  P. Latham,et al.  Retinal ganglion cells act largely as independent encoders , 2001, Nature.

[37]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[38]  Satoru Kato,et al.  Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina , 1983, Nature.

[39]  S. M. Wu,et al.  Feedforward lateral inhibition in retinal bipolar cells: input-output relation of the horizontal cell-depolarizing bipolar cell synapse. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[40]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[41]  F S Werblin,et al.  Three Levels of Lateral Inhibition: A Space–Time Study of the Retina of the Tiger Salamander , 2000, The Journal of Neuroscience.

[42]  L. Croner,et al.  Receptive fields of P and M ganglion cells across the primate retina , 1995, Vision Research.

[43]  R. Dacheux,et al.  Alpha ganglion cells of the rabbit retina lose antagonistic surround responses under dark adaptation , 1997, Visual Neuroscience.

[44]  P. Lennie,et al.  Spatial frequency analysis in the visual system. , 1985, Annual review of neuroscience.

[45]  L Maffei,et al.  Homeostasis in retinal receptive fields. , 1971, Journal of neurophysiology.

[46]  L. Maffei,et al.  Spatial frequency and orientation tuning curves of visual neurones in the cat: Effects of mean luminance , 1977, Experimental Brain Research.

[47]  D. Dacey,et al.  Receptive field structure of H1 horizontal cells in macaque monkey retina. , 2002, Journal of vision.

[48]  L. Pinto,et al.  Response properties of ganglion cells in the isolated mouse retina , 1993, Visual Neuroscience.

[49]  Paul Witkovsky,et al.  Chapter 10 Functional roles of dopamine in the vertebrate retina , 1991 .

[50]  Edward N. Pugh,et al.  From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG , 2004, Vision Research.

[51]  R. W. Rodieck Quantitative analysis of cat retinal ganglion cell response to visual stimuli. , 1965, Vision research.

[52]  R. G. Smith,et al.  Simulation of an anatomically defined local circuit: The cone-horizontal cell network in cat retina , 1995, Visual Neuroscience.

[53]  H. Wässle,et al.  Synaptic Currents Generating the Inhibitory Surround of Ganglion Cells in the Mammalian Retina , 2001, The Journal of Neuroscience.

[54]  R. Douglas,et al.  Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. , 2004, Investigative ophthalmology & visual science.

[55]  R. Weiler,et al.  pH-gated dopaminergic modulation of horizontal cell gap junctions in mammalian retina , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  J. Dowling,et al.  Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. , 1985, Science.

[57]  M Kamermans,et al.  Hemichannel-Mediated Inhibition in the Outer Retina , 2001, Science.

[58]  R M Douglas,et al.  Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system , 2005, Visual Neuroscience.

[59]  R. Jensen,et al.  Effects of dopamine and its agonists and antagonists on the receptive field properties of ganglion cells in the rabbit retina , 1986, Neuroscience.

[60]  K. Tornqvist,et al.  Modulation of cone horizontal cell activity in the teleost fish retina. III. Effects of prolonged darkness and dopamine on electrical coupling between horizontal cells , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  Timm Schubert,et al.  Functional expression of connexin57 in horizontal cells of the mouse retina , 2004, The European journal of neuroscience.

[62]  H. Barlow,et al.  Change of organization in the receptive fields of the cat's retina during dark adaptation , 1957, The Journal of physiology.

[63]  S. Kéri,et al.  Human scotopic spatiotemporal sensitivity: a comparison of psychophysical and electrophysiological data , 2003, Documenta Ophthalmologica.

[64]  J. Robson,et al.  Application of fourier analysis to the visibility of gratings , 1968, The Journal of physiology.

[65]  C. Cavonius,et al.  Relationships between luminance and visual acuity in the rhesus monkey , 1973, The Journal of physiology.

[66]  Michael J. Berry,et al.  Adaptation of retinal processing to image contrast and spatial scale , 1997, Nature.

[67]  D. I. Vaney,et al.  Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin , 1991, Neuroscience Letters.