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X. Cao, D. K. Merwine, N. M. Grzywacz; Asymmetric Responses of Retinal Ganglion Cells to the Onset and Offset of Natural Images. Invest. Ophthalmol. Vis. Sci. 2008;49(13):3860.
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When stimulated with artificial stimuli (such as spots or moving edges), On and Off retinal ganglion cells respond to receptive-field brightening and darkening respectively. We investigated whether the same occurs when using natural images.
We used multi-electrode arrays to record responses of rabbit’s retinal ganglion cells (RGCs). They were stimulated with back and forth transitions from homogeneously gray images to natural images with same mean luminance. We used regularized spike-triggered-average (rSTA) technique to obtain the RGC receptive fields (RF) for the further analysis
On cells only responded well to the appearance of natural images (i.e., transitions from gray to natural images). This was surprising because both 50% of appearances and 50% of disappearances (i.e., transitions from natural images to gray) brightened the RF on average. In contrast, Off cells only respond well to the disappearance of natural images. To probe this asymmetry further, RFs were estimated with rSTA for 121 cells. In the ensuing data, 15 of 17 On cells only showed clear On RF structure when stimulated with the appearance of natural images. In turn, 59 of 61 Off cells only showed clear Off structure with image disappearances. And 42 of 43 On-Off cells only showed clear On and Off structures for appearances and disappearances respectively. Finally, we tested whether these asymmetries were caused by the well-known asymmetric distribution of intensities in natural images. We performed experiments with both normal and contrast-reversed natural images. These experiments showed that the asymmetry in the images did not cause the asymmetric structures of RGCs by differential stimulation of On and Off mechanisms.
Our results suggest that On cells prefer the appearance of bright objects in natural scenes over the disappearance of dark objects. In turn, Off cells may prefer the disappearance of bright objects over the appearance of dark objects. Finally, On-Off cells seem to prefer the appearance and disappearance of bright objects over the appearance and disappearance dark objects. These asymmetries are not caused by differential stimulation due to the asymmetric distribution of intensities in natural images. Hence, the asymmetries contradict the common prediction that "the offset of a picture might be the same as the onset of its contrast-reversed image" (Smyth, 2003). One possible functional explanation for the asymmetry is that dark objects are often shadows in natural images. We propose a biophysical model based on horizontal-cell circuitry to explain the observed asymmetries.
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