The early visual system is endowed with adaptive mechanisms that rapidly adjust gain and integration time based on the local luminance (mean intensity) and contrast (standard deviation of intensity relative to the mean). Here we show that these mechanisms are matched to the statistics of the environment. First, we measured the joint distribution of luminance and contrast in patches selected from natural images and found that luminance and contrast were statistically independent of each other. This independence did not hold for artificial images with matched spectral characteristics. Second, we characterized the effects of the adaptive mechanisms in lateral geniculate nucleus (LGN), the direct recipient of retinal outputs. We found that luminance gain control had the same effect at all contrasts and that contrast gain control had the same effect at all mean luminances. Thus, the adaptive mechanisms for luminance and contrast operate independently, reflecting the very independence encountered in natural images.

/pdf/independence-of-luminance-and-contrast-in-natural-scenes-and-2ehoq8gmx9.pdf

Independence of luminance and contrast in natural scenes and in the early visual system

Lateral interactions in the outer retina

Ambient illumination toggles a neuronal circuit switch in the retina and visual perception at cone threshold.

Although the center-surround receptive field is a fundamental property of retinal ganglion cells, the circuitry that mediates surround inhibition remains controversial. We examined the contribution of horizontal cells and amacrine cells to the surround of parasol ganglion cells of macaque and baboon retina by measuring receptive field structure before and during the application of drugs that have been shown previously to affect surrounds in a range of mammalian and nonmammalian species. Carbenoxolone and cobalt, thought to attenuate feedback from horizontal cells to cones, severely reduced the surround. Tetrodotoxin, which blocks sodium spiking in amacrine cells, and picrotoxin, which blocks the inhibitory action of GABA, only slightly reduced the surround. These data are consistent with the hypothesis that the surrounds of light-adapted parasol ganglion cells are generated primarily by non-GABAergic horizontal cell feedback in the outer retina, with a small contribution from GABAergic amacrine cells of the inner retina.

https://www.jneurosci.org/content/jneuro/24/15/3736.full.pdf

The classical receptive field surround of primate parasol ganglion cells is mediated primarily by a non-GABAergic pathway.

https://www.cell.com/neuron/pdf/S0896-6273(08)00257-2.pdf

Functional Mechanisms Shaping Lateral Geniculate Responses to Artificial and Natural Stimuli

Our objective with this study was to provide a near complete characterization of how mean light level changes the spatial receptive-field properties of X-cells. Single X-cells were recorded extracellularly either from cell bodies in the retina or from their axons in the optic tract. Frequency responses of the cells at 2 Hz were measured for a set of gratings of different spatial frequencies and for a stimulus designed to probe the spatial properties of the receptive-field surround. Predicted frequency responses of a Gaussian center-surround model for the receptive field were fit simultaneously to both sets of measurements and the parameters of the model that best fit the data used to characterize the spatial properties of the receptive field. Measurements were made at a number of mean light levels for each cell and changes in receptive-field properties were characterized by changes in the parameters of the Gaussian center-surround model. The range of illuminances studied covered the bulk of the range encountered by a cat naturally and three distinct functional ranges appeared to express themselves in the data. One range corresponded to the cat's photopic range of vision. The other two ranges were where signals originating in rods dominate X-cell responses. We argue that one corresponds to the range that rod signals pass predominantly through rod bipolars en route to the X-cell, while the other is where rod signals flow predominantly through cones via gap junctions and then follow the path of cone signals to the X-cell. Among the major findings are that Weber's Law is followed throughout the photopic but not the scotopic range, that center radius expands under scotopic conditions, and that the surround is present even at the lowest scotopic levels we studied.

Spatial properties of the cat X-cell receptive field as a function of mean light level.

Technical measurements of the Sony Multiscan 17se were made and are reported in the belief that they would be useful to visual scientists who consider employing this device as a display unit. Luminance, spatial uniformity, luminance additivity between the output of the guns, CIE1931 chromaticity coordinates, and gamma correction parameters were measured. The characteristics of individual monitors will probably be different from the one studied here but it is believed that the results obtained serve as a fair indication of what might be expected from this device.

Characteristics of the Sony Multiscan 17se Trinitron color graphic display

Pupillary area was measured in urethane-anesthetized cats as a function of retinal illuminance. When appropriate corrections are made for differences in experimental procedures, it was found that the pupillary response of the urethane-anesthetized cat's eyes to light was basically unchanged from that of the alert behaving cat. This preparation may therefore be a very satisfactory one in which to study the pupillary response pathway in a higher mammal.

The cat's pupillary light response under urethane anesthesia

Visual responses to stimulation at high temporal frequency are generally considered to result from signals that avoid light adaptive gain adjustment, simply reflecting linear summation of luminance. Under conditions of high photopic illuminance, the center of the receptive field of the cat X-cell has been shown to expand in size when stimulated at high temporal frequency, raising the possibility that there is spatiotemporal interaction in luminance summation. Here we show that this expansion maintains constant the product of the center's luminance summing area and the temporal period of luminance modulation, implying that spatial and temporal integration of luminance can be traded for one another by the X-cell center. As such the X-cell has a spatiotemporal window for luminance integration that fuses the classical concepts of a spatial window of luminance integration (Ricco's Law) with a temporal window of luminance integration (Bloch's Law). We were interested to determine whether this tradeoff between spatial and temporal summation of luminance occurs also at lower light levels, where the temporal-frequency bandwidth of the X-cell is narrower. We found that it does not. Center radius does not expand with temporal frequency under either low photopic or scotopic conditions. These results are discussed within the context of the known retinal circuitry that underlies the X-cell center for photopic and scotopic conditions.

/pdf/spatiotemporal-integration-of-light-by-the-cat-x-cell-center-1jthpy0d48.pdf

Spatiotemporal integration of light by the cat X-cell center under photopic and scotopic conditions.

VSApc is a suite of DOS programs that was developed to measure spatiotemporal frequency responses and to collect maintained discharge from retinal ganglion cells of cats and monkeys. The operation of the programs is described and their details summarized.

D. L. Bohnsack

Papers

Spatial properties of the cat X-cell receptive field as a function of mean light level.

Characteristics of the Sony Multiscan 17se Trinitron color graphic display

The cat's pupillary light response under urethane anesthesia

Spatiotemporal integration of light by the cat X-cell center under photopic and scotopic conditions.

VSApc: a C++ package for quantitative extracellular single-cell electrophysiology.