Center-surround organization in bipolar cells: Symmetry for opposing contrasts

Abstract

Intracellular recordings were obtained from 73 cone-driven bipolar cells in the light-adapted retina of the tiger salamander (Ambystoma tigrinum). Responses to flashes of negative and positive contrast for centered spots and concentric annuli of optimum spatial dimensions were analyzed as a function of contrast magnitude. For both depolarizing and hyperpolarizing bipolar cells, it was found that remarkably similar responses were observed for the center and surround when comparisons were made between responses of the same response polarity and thus, responses to opposite contrast polarity. Thus, spatial information and contrast polarity appear to be rather strongly confounded in many bipolar cells. As a rule, the form of the contrast/response curves for center and surround approximated mirror images of each other. Contrast gain and C50 (the contrast required for half-maximal response) were quantitatively similar for center and surround when comparisons were made for responses of the same response polarity. The average contrast gain of the bipolar cell surround was 3-5 times higher than that measured for horizontal cells. Contrast/latency measurements and interactions between flashed spots and annuli showed that the surround response is delayed by 20-80 ms with respect to that of the receptive-field center. Cones showed no evidence for center-surround antagonism while for bipolar cells, the average strength of the surround ranged from about 50% to 155% of the center, depending on the test and response polarity. The results of experiments on the effects of APB (100 microM) on depolarizing bipolar cells suggest that the relative contribution of the feedback pathway (horizontal cell to cones) and the feedforward pathway (horizontal cell to bipolar cell) to the bipolar surround varies in a distributed manner across the bipolar cell population.

Contrast processing by ON and OFF bipolar cells

“…We found that the response of the surround was delayed by about 50 ms with respect to that of the receptive field center, a finding consistent with the common view that the surround response is mediated by slower mechanisms than that of the center. The cone voltage showed no evidence for center-surround antagonism (Fahey & Burkhardt, 2003) in agreement with Hare and Owen (1992). This finding is compatible with the view that surround antagonism is due to modulation of calcium currents in the cone pedicle due to feedback from horizontal cells and is not normally detectable in the cone photovoltage Thoreson et al, 2008) .…”

“…We believe that our work (Fahey & Burkhardt, 2003) is the first to systematically investigate the full contrastresponse curves for both negative and positive contrasts for both center and surround. In our sample, the size of the center ranged from about 100-500 lm in diameter across the bipolar population in both ON and OFF bipolars (see also Hare & Owen, 1990;Zhang & Wu, 2009).…”

Ionotropic GABA Receptors and Distal Retinal ON and OFF Responses

“…The ineffectiveness of the GABA antagonists to eliminate the surround responses of the OFF bipolar cells in these experiments may be due to inappropriate light adaptation conditions. The retina has been maintained under mid to high scotopic illumination conditions, while the bipolar cell surround responses are strongest under light adapted conditions [207, 208]. To reveal the role of the GABAergic system in the centre-surround organization of cone ON and OFF bipolar cells, the effects of GABA receptor antagonists should be determined under maintained light adapted conditions.…”

Dopamine Regulation of GABAA Receptors Contributes to Light/Dark Modulation of the ON-Cone Bipolar Cell Receptive Field Surround in the Retina

“…First, following maintained (30 min) bright background illumination, stimulation of the RF surround alone using an annulus or ring of light produces a response that is opposite in polarity to that produced by center (spot) stimulation alone, a phenomenon called “surround activation,” and surround stimulation in the presence of center stimulation using spot and annulus together reduces the amplitude of the center response, a phenomenon called “surround antagonism” [1–8]. Second, although cBC and GC surround responses are strongest under maintained bright background illumination, surround strength progressively decreases as the light level decreases so that the surround is minimal following maintained darkness [7–12]. This adaptive process likely contributes to modulation of the spatial discrimination ability of human and monkey observers by the ambient light level [13].…”