Why the Eye Is Better Than a Camera at Capturing Contrast and Faint Detail Simultaneously
ScienceDaily (May 3, 2011) — The human eye long ago solved a problem common to both digital and film cameras: how to get good contrast in an image while also capturing faint detail.
Cones normally release the neurotransmitter glutamate in the dark, while light decreases glutamate release. This graph of neurotransmitter release shows what happens when cone cells are exposed to a dark spot in a light background (top) under various scenarios, including no feedback (green trace) and only negative feedback from horizontal cells (red trace). Negative feedback to many cones enhances edges, but would decrease detail in dark areas were it not for newly discovered positive feedback that is localized to only a few cone cells (blue trace). (Credit: Richard Kramer lab, UC Berkeley)
Nearly 50 years ago, physiologists described the retina's tricks for improving contrast and sharpening edges, but new experiments by University of California, Berkeley, neurobiologists show how the eye achieves this without sacrificing shadow detail.
"One of the big success stories, and the first example of information processing by the nervous system, was the discovery that the nerve cells in the eye inhibit their neighbors, which allows the eye to accentuate edges," said Richard Kramer, UC Berkeley professor of molecular and cell biology. "This is great if you only care about edges. But we also want to know about the insides of objects, especially in dim light."
Kramer and former graduate student Skyler L. Jackman, now a post-doctoral fellow at Harvard University, discovered that while light-sensitive nerve cells in the retina inhibit dozens of their close neighbors, they also boost the response of the nearest one or two nerve cells.
That extra boost preserves the information in individual light detecting cells -- the rods and cones -- thereby retaining faint detail while accentuating edges, Kramer said. The rods and cones thus get both positive and negative feedback from their neighbors.
"By locally offsetting negative feedback, positive feedback boosts the photoreceptor signal while preserving contrast enhancement," he said.
Jackman, Kramer and their colleagues at the University of Nebraska Medical Center in Omaha report their findings May 3 in the journal PLoS Biology. Kramer also will report the findings at the 2011 annual meeting of the Association for Research in Vision and Ophthalmology in Ft. Lauderdale, Fla....
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A Positive Feedback Synapse from Retinal Horizontal Cells to Cone Photoreceptors
1 Department of Physics, University of California, Berkeley, Berkeley, California, United States of America, 2 Department of Ophthalmology, University of Nebraska Medical Center, Omaha, Nebraska, United States of America, 3 Department of Chemistry, University of Massachusetts, Amherst, Amherst, Massachusetts, United States of America, 4 Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California, United States of America
Abstract
Cone photoreceptors and horizontal cells (HCs) have a reciprocal synapse that underlies lateral inhibition and establishes the antagonistic center-surround organization of the visual system. Cones transmit to HCs through an excitatory synapse and HCs feed back to cones through an inhibitory synapse. Here we report that HCs also transmit to cone terminals a positive feedback signal that elevates intracellular Ca2+and accelerates neurotransmitter release. Positive and negative feedback are both initiated by AMPA receptors on HCs, but positive feedback appears to be mediated by a change in HC Ca2+, whereas negative feedback is mediated by a change in HC membrane potential. Local uncaging of AMPA receptor agonists suggests that positive feedback is spatially constrained to active HC-cone synapses, whereas the negative feedback signal spreads through HCs to affect release from surrounding cones. By locally offsetting the effects of negative feedback, positive feedback may amplify photoreceptor synaptic release without sacrificing HC-mediated contrast enhancement.
Author Summary
Visual images are projected by the lens of the eye onto a sheet of photoreceptor cells in the retina called rods and cones. Like the pixels in a digital camera, each photoreceptor generates an electrical response proportional to the local light intensity. Each photoreceptor then initiates a chemical signal that is transmitted to downstream neurons, ultimately reaching the brain. But unlike the pixels of a digital camera, photoreceptors indirectly inhibit one another through laterally projecting horizontal cells. Horizontal cells integrate signals from many photoreceptors and provide inhibitory feedback. This feedback is thought to underlie “lateral inhibition,” a process that sharpens our perception of contrast and color. Here we report the surprising finding that horizontal cells also provide positive feedback to photoreceptors, utilizing a mechanism distinct from negative feedback. The positive feedback signal is constrained to individual horizontal cell–photoreceptor connections, whereas the negative feedback signal spreads throughout a horizontal cell to affect many surrounding photoreceptors. By locally offsetting negative feedback, positive feedback boosts the photoreceptor signal while preserving contrast enhancement.
Citation: Jackman SL, Babai N, Chambers JJ, Thoreson WB, Kramer RH (2011) A Positive Feedback Synapse from Retinal Horizontal Cells to Cone Photoreceptors. PLoS Biol 9(5): e1001057. doi:10.1371/journal.pbio.1001057
Academic Editor: Fred Rieke, University of Washington, United States of America
Received: November 26, 2010; Accepted: March 25, 2011; Published: May 3, 2011
Copyright: © 2011 Jackman et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by grants from the National Institutes of Health EY015514 and EY018957 (RHK), EY10542 (WBT), Research to Prevent Blindness (WBT), and the Human Frontiers Science Program (JCC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: CBO, carbenoxolone; CNG, cyclic nucleotide-gated; HC, horizontal cell; INL, inner nuclear layer; IPC, interplexiform cell; IPL, inner plexiform layer; mEPSC, miniature excitatory postsynaptic current; NO, nitric oxide; NOS, NO synthase; sGC, soluble guanylate cyclase
* E-mail: rhkramer@berkeley.edu
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