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Why the eye is better than a camera


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. Nearly 50 years ago, physiologists described the retina's tricks for improving contrast and sharpening edges, but new experiments by neurobiologists at University of California, Berkeley and the University of Nebraska Medical Center in Omaha show how the eye achieves this without sacrificing shadow detail. These details will be published next week in the online, open access journal PLoS Biology.

"Lateral inhibition" (when light-sensitive nerve cells in the retina inhibit dozens of their near neighbors) was first observed in horseshoe crabs by physiologist H. Keffer Hartline. This form of negative feedback was later shown to take place in the vertebrate eye, including the human eye, and has since been found in many sensory systems as a way to sharpen the discrimination of pitch or touch. Lateral inhibition fails, however, to account for the eye's ability to detect faint detail near edges, including the fact that we can see small, faint spots which ought to be invisible if their detection is inhibited by encircling retinal cells.

The retina in vertebrates is lined with a sheet of photoreceptor cells: the cones for day vision and the rods for night vision. The lens of the eye focuses images onto this sheet, and like the pixels in a digital camera, each photoreceptor generates an electrical response proportional to the intensity of the light falling on it. The signal releases a chemical neurotransmitter (glutamate) that affects neurons downstream, ultimately reaching the brain. Unlike the pixels of a digital camera, however, photoreceptors affect the photoreceptors around them through so-called horizontal cells, which underlie and touch as many as 100 individual photoreceptors. The horizontal cells integrate signals from all these photoreceptors and provide broad inhibitory feedback. This feedback is thought to underlie lateral inhibition.

In the current study, Richard Kramer and former graduate student Skyler L. Jackman discovered that during lateral inhibition, horizontal cells not only inhibit their neighbors (negative feedback), but also boost the response of the nearest cells (positive feedback). That extra boost preserves the information in individual light detecting cells the rods and cones thereby retaining faint detail while accentuating edges. By locally offsetting negative feedback, positive feedback boosts the photoreceptor signal while preserving contrast enhancement. Positive feedback is local, whereas negative feedback extends laterally, enhancing contrast between center and surround.

The researchers also found that the two types of feedback work by different mechanisms. Traditional negative feedback uses electrical signals that propagate from horizontal cells to many nearby photoreceptors. The positive feedback, however, involves chemical signaling. When a horizontal cell receives glutamate from a photoreceptor, calcium ions flow into the horizontal cell. These ions trigger the horizontal cell to "talk back" to the photoreceptor, Kramer said. Because calcium doesn't spread very far within the horizontal cell, the positive feedback signal stays local, affecting only one or two nearby photoreceptors.

Jackman and Kramer found the same positive feedback in the cones of a zebrafish, lizard, salamander, anole (whose retina contains only cones) and rabbit, proving that "this is not just some weird thing that happens in lizards; it seems to be true across all vertebrates and presumably humans."


Coauthors with Kramer and Jackman are Norbert Babai and Wallace B. Thoreson of the Department of Ophthalmology at the University of Nebraska Medical Center and James J. Chambers of the Department of Chemistry at the University of Massachusetts, Amherst.

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 statement: The authors declare that no competing interests exist.

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