Effects of light adaptation on contrast processing in bipolar cells in the retina

Abstract

Effects of light adaptation on contrast processing in the outer retina were investigated over nearly four decades of background illumination by analyzing the intracellular responses of 111 bipolar cells, 66 horizontal cells, and 22 cone photoreceptors in the superfused eyecup of the tiger salamander (Ambystoma tigrinum). Light adaptation had striking and similar effects on the average contrast responses of the hyperpolarizing (Bh) and depolarizing (Bd) classes of bipolar cells: Over the lower two decades of background illumination, the contrast gain increased 7-fold to reach values as high as 20-30, the dynamic range and the half-maximum contrast decreased by about 60%, the total voltage range increased some 40%, and contrast dominance changed from highly positive to more balanced. At higher levels of background, most aspects of the contrast response stabilized and Weber's Law then held closely. In this background range, the contrast gain of bipolar cells was amplified some 20X relative to that of cones whereas the corresponding amplification in horizontal cells was about 6X. Differences in the growth of contrast gain with the intensity of the background illumination for cones versus bipolar cells suggest that there are at least two adaptation-dependent mechanisms regulating contrast gain. One is evident in the cone photoresponse such that an approximately linear relation holds between the steady-state hyperpolarization and contrast gain. The other arises between the voltage responses of the cones and bipolar cells. It could be presynaptic (modulation of cone transmitter release by horizontal cell feedback or other mechanisms) and/or postsynaptic, that is, intrinsic to bipolar cells. Contrast gain grew with the background intensity by a larger factor in horizontal than in bipolar cells. This provides a basis for the widely held view that light adaptation increases the strength of surround antagonism in bipolar cells. On average, the effects of light adaptation and most quantitative indices of contrast processing were remarkably similar for Bd and Bh cells, implying that both classes of bipolar cells, despite possible differences in underlying mechanisms, are about equally capable of encoding all primary aspects of contrast at all levels of light adaptation.

Ambient Light Regulates Sodium Channel Activity to Dynamically Control Retinal Signaling

“…2C), although the resting membrane potential was adjusted with current injection to ensure that voltage-gated channels were similarly activated (dim, Ϫ57.7 Ϯ 1.8 mV; bright, Ϫ56.0 Ϯ 2.7 mV; p ϭ 0.30). Because bright background light can depolarize salamander ON bipolar cells (3-5 mV) (Werblin, 1974;Fahey and Burkhardt, 2001), the sodium current contributions in bright-light conditions were probably overestimated because of sodium channel inactivation at more positive potentials (Ichinose et al, 2005). These findings indicate that sodium channels did not boost L-EPSPs in bright conditions (Fig.…”

“…3), and the estimated Na ϩ conductance during a similar magnitude of L-EPSP is 0 nS, which produces no enhancement. However, if bright-light conditions depolarize the bipolar cell to a resting potential of Ϫ50 mV (Werblin, 1974;Fahey and Burkhardt, 2001), then the estimated magnitude of the Na ϩ conductance during an L-EPSP (depolarization from Ϫ50 to Ϫ40 mV) is 0.0025 nS, attributable to more activation and inactivation of the Na ϩ channels (Fig. 3).…”

Contrast encoding in retinal bipolar cells: Current vs. voltage

“…When the retina is light adapted to background illumination of 20 cd0m 2 , the bipolar cells are predominately driven by the red-sensitive (610 nm) cones, contrast sensitivity is high, approaching the maximal attainable level, and flashes presented at intervals of 5-10 s do not alter the state of light adaptation (Fahey & Burkhardt, 2001). Therefore, in the present work, the background was set at 20 cd0m 2 and responses were evoked with 5-10 s between flashes.…”

“…Custom software described previously Fahey & Burkhardt, 2001) was used to control the light transmitted by the LCD. The light output was held at a steady "background" level.…”

A high frequency resonance in the responses of retinal ganglion cells to rapidly modulated stimuli: A computer model

“…While the responses to temporally modulated stimuli are often complex (Reich et al, 1997), the band-pass character of ganglion cell tMTFs below approximately 40 Hz can be largely explained by a combination of known mechanisms. Adaptation, present at all stages of retinal processing (Frishman & Sieving, 1995;Shapley, 1997;Fahey & Burkhardt, 2001;Hurley, 2002), will suppress ganglion cell responses to slowly varying stimuli. Likewise, responses to rapidly varying stimuli will be suppressed by a variety of low-pass filtering mechanisms, including the finite time constants of retinal neurons (O'Brien et al, 2002) as well as the finite duration of the phototransduction process (Schnapf et al, 1990).…”