Natural images and contrast encoding in bipolar cells in the retina of the land- and aquatic-phase tiger salamander

Burkhardt, Dwight A.; Fahey, Patrick K.; Sikora, Michael

doi:10.1017/s0952523806231043

Cited by 31 publications

(41 citation statements)

References 26 publications

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“…Thus, the fraction of dark contrasts exceeded the fraction of bright contrasts even without divisive normalization. These findings extend early reports of specific instances of a skew to negative contrasts (15,28,29).…”

supporting

confidence: 90%

Retina is structured to process an excess of darkness in natural scenes

Ratliff

Borghuis

Kao

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

190

215

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Retinal ganglion cells that respond selectively to a dark spot on a brighter background (OFF cells) have smaller dendritic fields than their ON counterparts and are more numerous. OFF cells also branch more densely, and thus collect more synapses per visual angle. That the retina devotes more resources to processing dark contrasts predicts that natural images contain more dark information. We confirm this across a range of spatial scales and trace the origin of this phenomenon to the statistical structure of natural scenes. We show that the optimal mosaics for encoding natural images are also asymmetric, with OFF elements smaller and more numerous, matching retinal structure. Finally, the concentration of synapses within a dendritic field matches the information content, suggesting a simple principle to connect a concrete fact of neuroanatomy with the abstract concept of information: equal synapses for equal bits.ganglion cells | neural coding | vision T he brain separates light from dark unequally. Psychophysical studies and measurements of visually evoked potentials show greater sensitivity to light decrements and dark spots in images (1, 2). Also, more cortical cells respond to negative than positive contrasts (3). In fact, this asymmetry begins with the second order (bipolar) neurons in the retina, which rectify the local contrast signal from the cone array (Fig. 1A). OFF cone bipolar cells (responding mostly to negative contrasts) outnumber the ON cells (responding mostly to positive contrasts) by 2-fold (4); thus, right from the start, the brain provides more resources for signaling negative contrasts.This aspect of retinal structure continues through the ganglion-cell level, where some ganglion-cell types have paired ON and OFF polarities (e.g., P and M in monkey, brisk-transient and brisk-sustained in rabbit and guinea pig, and X and Y in cat). Of these, the OFF cells have narrower dendritic fields and correspondingly narrower receptive-field centers than their ON partners [guinea pig (Fig. 1B), rat (5), rabbit (6), monkey (7), human (8), and smaller differences in cat (9)]. Thus, to cover the retina, OFF cells outnumber their ON partners. OFF arbors are narrower across cell classes with different spatiotemporal bandwidths (e.g., they are narrower for both midget and parasol cells in humans) (8). Specifically, whereas in fovea, midget cells are paired (one ON and one OFF per cone), beyond fovea, where midget cells collect from many bipolar cells and cones, OFF cells have smaller arbors and hence, are more numerous.While OFF cells distribute more densely than their counterpart ON cells, both types have similar receptive-field overlap (spacing is about two times the SD of a Gaussian fit to the central receptive field) (6, 10, 11). Furthermore, OFF arbors (as we quantify here) branch more densely (5) and provide similar dendritic membrane areas as ON arbors. Because the membrane density of excitatory synapses (synapses/μm 2 ) is constant across an arbor and across cell types (12, 13), OFF cells receive simi...

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supporting

confidence: 90%

Retina is structured to process an excess of darkness in natural scenes

Ratliff

Borghuis

Kao

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

190

215

View full text Add to dashboard Cite

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“…This evidence for matched amplification provides a new view for the function of light adaptation and the contribution of the cone-bipolar synapse in vertebrate vision. Work to date suggests that our results for contrast flashes also apply to image movement on the retina (Burkhardt et al, 2006).…”

Section: Distributed Coding In Bipolar Cells and Natural Imagesmentioning

confidence: 61%

“…Although the retina of the aquatic-phase salamander has been studied extensively for some four decades by many investigators, no reports were known for land-phase animals. We found, on average, that the contrast-response curves of ON and OFF bipolar cells in the landphase animals were remarkably similar to those of aquatic-phase animals (Burkhardt et al, 2006). Thus, the primary retinal mechanisms mediating contrast coding in the outer retina remain functionally stable as the salamander evolves from the aquatic to the land phase.…”

Section: Distributed Coding In Bipolar Cells and Natural Imagesmentioning

confidence: 69%

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Contrast processing by ON and OFF bipolar cells

Burkhardt

2010

Vis Neurosci

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Much of what is currently known about the visual response of retinal bipolar cells is based on studies of rod-dominant responses to flashes in the dark in the isolated retina. This minireview summarizes quantitative findings on contrast processing in the intact light-adapted retina based on intracellular recording from more than 400 cone-driven bipolar cells in the tiger salamander: 1) In the main, the contrast responses of ON and OFF cells are surprisingly similar, suggesting a need to refine the view that ON and OFF cells provide the selective substrates for processing of positive and negative contrasts, respectively. 2) Overall, the response is quite nonlinear, showing very high gain for small contrasts, some 10-15 times greater than that of cones, but then quickly approaches saturation for higher contrasts. 3) Under optimal conditions of light adaptation, both classes of bipolar cells show evidence for efficient coding with respect to the contrasts in natural images. 4) There is a marked diversity within both the ON and OFF bipolar cell populations and an absence of discrete subtypes. The dynamic ranges bracket the range of contrasts in nature. 5) For both ON and OFF cells, the receptive field organization shows a striking symmetry between center and surround for responses of the same polarity and thus opposite contrast polarities. 6) The latency difference between ON and OFF cells is about 30 ms, which seems qualitatively consistent with a delay due to the G-protein cascade in ON bipolar cells. 7) In sum, we report quantitative evidence for at least 11 transformations in signal processing that occur between the voltage response of cones and the voltage response of bipolar cells.

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“…Ganglion cells with response properties similar to those of the fast-OFF cells studied in our larval salamanders have also been explored in a variety of other amphibians and mammals (Lettvin et al, 1959;Shapley and Victor, 1978;Berry et al, 1999;Petrusca et al, 2007), and are presumably found in both the larval and adult form of the tiger salamander. Indeed, contrast coding in the outer retina of larval tiger salamanders has been shown to be functionally equivalent to that in terrestrial adults (Burkhardt et al, 2006). For these reasons, we believe that the larval tiger salamander is both a representative and experimentally accessible system in which to begin studying the motion processing experienced by both aquatic and terrestrial amphibians.…”

Section: Methodsmentioning

confidence: 96%

Nonlinear Dynamics Support a Linear Population Code in a Retinal Target-Tracking Circuit

Leonardo

Meister

2013

J. Neurosci.

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A basic task faced by the visual system of many organisms is to accurately track the position of moving prey. The retina is the first stage in the processing of such stimuli; the nature of the transformation here, from photons to spike trains, constrains not only the ultimate fidelity of the tracking signal but also the ease with which it can be extracted by other brain regions. Here we demonstrate that a population of fast-OFF ganglion cells in the salamander retina, whose dynamics are governed by a nonlinear circuit, serve to compute the future position of the target over hundreds of milliseconds. The extrapolated position of the target is not found by stimulus reconstruction but is instead computed by a weighted sum of ganglion cell outputs, the population vector average (PVA). The magnitude of PVA extrapolation varies systematically with target size, speed, and acceleration, such that large targets are tracked most accurately at high speeds, and small targets at low speeds, just as is seen in the motion of real prey. Tracking precision reaches the resolution of single photoreceptors, and the PVA algorithm performs more robustly than several alternative algorithms. If the salamander brain uses the fast-OFF cell circuit for target extrapolation as we suggest, the circuit dynamics should leave a microstructure on the behavior that may be measured in future experiments. Our analysis highlights the utility of simple computations that, while not globally optimal, are efficiently implemented and have close to optimal performance over a limited but ethologically relevant range of stimuli.

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Natural images and contrast encoding in bipolar cells in the retina of the land- and aquatic-phase tiger salamander

Cited by 31 publications

References 26 publications

Retina is structured to process an excess of darkness in natural scenes

Retina is structured to process an excess of darkness in natural scenes

Contrast processing by ON and OFF bipolar cells

Nonlinear Dynamics Support a Linear Population Code in a Retinal Target-Tracking Circuit

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