Lateral Gain Control in the Outer Retina Leads to Potentiation of Center Responses of Retinal Neurons

The retina can function under a variety of adaptation conditions and stimulus paradigms. To adapt to these various conditions, modifications in the phototransduction cascade and at the synaptic and network levels occur. In this paper, we focus on the properties and function of a gain control mechanism in the cone synapse. We show that horizontal cells, in addition to inhibiting cones via a “lateral inhibitory pathway,” also modulate the synaptic gain of the photoreceptor via a “lateral gain control mechanism.” The combination of lateral inhibition and lateral gain control generates a highly efficient transformation. Horizontal cells estimate the mean activity of cones. This mean activity is subtracted from the actual activity of the center cone and amplified by the lateral gain modulation system, ensuring that the deviation of the activity of a cone from the mean activity of the surrounding cones is transmitted to the inner retina with high fidelity. Sustained surround illumination leads to an enhancement of the responses of transient ON/OFF ganglion cells to a flickering center spot. Blocking feedback from horizontal cells not only blocks the lateral gain control mechanism in the outer retina, but it also blocks the surround enhancement in transient ON/OFF ganglion cells. This suggests that the effects of the outer retinal lateral gain control mechanism are visible in the responses of ganglion cells. Functionally speaking, this result illustrates that horizontal cells are not purely inhibitory neurons but have a role in response enhancement as well.

[1]  D. A. Burkhardt,et al.  Sensitization and centre‐surround antagonism in Necturus retina , 1974, The Journal of physiology.

[2]  H. Spekreijse,et al.  Horizontal cells feed back to cones by shifting the cone calcium-current activation range , 1996, Vision Research.

[3]  M. J. M. Lankheet,et al.  The lateral spread of light adaptation in cat horizontal cell responses , 1993, Vision Research.

[4]  Daniel Tranchina,et al.  Gain of Rod to Horizontal Cell Synaptic Transfer: Relation to Glutamate Release and a Dihydropyridine-Sensitive Calcium Current , 1997, The Journal of Neuroscience.

[5]  H Spekreijse,et al.  The dynamic characteristics of the feedback signal from horizontal cells to cones in the goldfish retina , 2001, The Journal of physiology.

[6]  Joseph J Atick,et al.  Could information theory provide an ecological theory of sensory processing? , 2011, Network.

[7]  J. Victor.  The dynamics of the cat retinal X cell centre. , 1987, The Journal of physiology.

[8]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[9]  Wallace B. Thoreson,et al.  Synaptic transmission at retinal ribbon synapses , 2005, Progress in Retinal and Eye Research.

[10]  Barry B. Lee,et al.  Dynamics of sensitivity regulation in primate outer retina: the horizontal cell network. , 2003, Journal of vision.

[11]  Markus Meister,et al.  Retina versus Cortex Contrast Adaptation in Parallel Visual Pathways , 2004, Neuron.

[12]  Kerry J. Kim,et al.  Temporal Contrast Adaptation in the Input and Output Signals of Salamander Retinal Ganglion Cells , 2001, The Journal of Neuroscience.

[13]  J. Pokorny,et al.  Horizontal cells reveal cone type-specific adaptation in primate retina. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  P. Ahnelt,et al.  Background-induced flicker enhancement in cat retinal horizontal cells. I. Temporal and spectral properties. , 1990, Journal of neurophysiology.

[15]  S. Baer,et al.  Background-induced flicker enhancement in cat retinal horizontal cells. II. Spatial properties. , 1990, Journal of neurophysiology.

[16]  D. Tranchina,et al.  Kinetics of synaptic transfer from rods and cones to horizontal cells in the salamander retina , 2003, Neuroscience.

[17]  H Spekreijse,et al.  Lateral feedback from monophasic horizontal cells to cones in carp retina. I. Experiments , 1989, The Journal of general physiology.

[18]  J. V. van Hateren.  A model of spatiotemporal signal processing by primate cones and horizontal cells. , 2007, Journal of vision.

[19]  J. B. Demb,et al.  Presynaptic Mechanism for Slow Contrast Adaptation in Mammalian Retinal Ganglion Cells , 2006, Neuron.

[20]  H. Spekreijse,et al.  Intrinsic Cone Adaptation Modulates Feedback Efficiency from Horizontal Cells to Cones , 1999, The Journal of general physiology.

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

[22]  F. Werblin.  Control of Retinal Sensitivity II. Lateral Interactions at the Outer Plexiform Layer , 1974 .

[23]  Akimichi Kaneko,et al.  pH Changes in the Invaginating Synaptic Cleft Mediate Feedback from Horizontal Cells to Cone Photoreceptors by Modulating Ca2+ Channels , 2003, The Journal of general physiology.

[24]  H Spekreijse,et al.  Spectral sensitivity of the feedback signal from horizontal cells to cones in goldfish retina , 1998, Visual Neuroscience.

[25]  C. Jacques,et al.  The time course of the inversion effect during individual face discrimination. , 2007, Journal of vision.

[26]  S. Laughlin,et al.  Predictive coding: a fresh view of inhibition in the retina , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

[28]  Hans van Hateren.  A cellular and molecular model of response kinetics and adaptation in primate cones and horizontal cells. , 2005, Journal of vision.

[29]  Tomomi Ichinose,et al.  Inner and outer retinal pathways both contribute to surround inhibition of salamander ganglion cells , 2005, The Journal of physiology.

[30]  D. Copenhagen,et al.  Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus). , 1988, The Journal of physiology.

[31]  H Barlow,et al.  Redundancy reduction revisited , 2001, Network.

[32]  S. Wu,et al.  Synaptic transmission in the outer retina. , 1994, Annual review of physiology.

[33]  M. Piccolino,et al.  Pre- and post-synaptic effects of manipulating surface charge with divalent cations at the photoreceptor synapse , 2004, Neuroscience.

[34]  A. Kaneko,et al.  Blocking effects of cobalt and related ions on the gamma‐aminobutyric acid‐induced current in turtle retinal cones. , 1986, The Journal of physiology.

[35]  Martin Wilson,et al.  Signal clipping by the rod output synapse , 1987, Nature.

[36]  P. Witkovsky,et al.  Feedback from luminosity horizontal cells mediates depolarizing responses of chromaticity horizontal cells in the Xenopus retina. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[37]  F. Werblin,et al.  Control of Retinal Sensitivity: I. Light and Dark Adaptation of Vertebrate Rods and Cones , 1974 .

[38]  F. Werblin,et al.  The response properties of the steady antagonistic surround in the mudpuppy retina. , 1978, The Journal of physiology.

[39]  H Spekreijse,et al.  The cone/horizontal cell network: A possible site for color constancy , 1998, Visual Neuroscience.

[40]  K. Yau,et al.  Phototransduction mechanism in retinal rods and cones. The Friedenwald Lecture. , 1994, Investigative ophthalmology & visual science.

[41]  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.

[42]  H. Spekreijse,et al.  Lateral feedback from monophasic horizontal cells to cones in carp retina. II. A quantitative model , 1989, The Journal of general physiology.

[43]  M. Kamermans,et al.  Cobalt ions inhibit negative feedback in the outer retina by blocking hemichannels on horizontal cells , 2004, Visual Neuroscience.