A novel mechanism of cone photoreceptor adaptation

Abstract

An animal’s ability to survive depends on its sensory systems being able to adapt to a wide range of environmental conditions, by maximizing the information extracted and reducing the noise transmitted. The visual system does this by adapting to luminance and contrast. While luminance adaptation can begin at the retinal photoreceptors, contrast adaptation has been shown to start at later stages in the retina. Photoreceptors adapt to changes in luminance over multiple time scales ranging from tens of milliseconds to minutes, with the adaptive changes arising from processes within the phototransduction cascade. Here we show a new form of adaptation in cones that is independent of the phototransduction process. Rather, it is mediated by voltage-gated ion channels in the cone membrane and acts by changing the frequency response of cones such that their responses speed up as the membrane potential modulation depth increases and slow down as the membrane potential modulation depth decreases. This mechanism is effectively activated by high-contrast stimuli dominated by low frequencies such as natural stimuli. However, the more generally used Gaussian white noise stimuli were not effective since they did not modulate the cone membrane potential to the same extent. This new adaptive process had a time constant of less than a second. A critical component of the underlying mechanism is the hyperpolarization-activated current, Ih, as pharmacologically blocking it prevented the long- and mid- wavelength sensitive cone photoreceptors (L- and M-cones) from adapting. Consistent with this, short- wavelength sensitive cone photoreceptors (S-cones) did not show the adaptive response, and we found they also lacked a prominent Ih. The adaptive filtering mechanism identified here improves the information flow by removing higher-frequency noise during lower signal-to-noise ratio conditions, as occurs when contrast levels are low. Although this new adaptive mechanism can be driven by contrast, it is not a contrast adaptation mechanism in its strictest sense, as will be argued in the Discussion.

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

“…The LN cascade modeling analysis in Figure 4 allowed us to compare different forms of center-surround integration, but these models do not capture all the relevant mechanisms shaping a RGC’s excitatory synaptic input. For example, history-dependent mechanisms like contrast and luminance adaptation probably substantially shape responses in a manner that these simple LN models cannot account for ( Demb, 2008 ; Howlett et al, 2017 ). Other work has explored predictive models that can account for history-dependent mechanisms and thereby out-perform simpler LN models ( Howlett et al, 2017 ; Cui et al, 2016 ; Ozuysal and Baccus, 2012 ).…”

Degenerated Cones in Cultured Human Retinas Can Successfully Be Optogenetically Reactivated

“…We also observed I h (Figure 3d), which is another major current commonly observed in vertebrate cones such as from goldfish [63], salamander [40], monkey [64] and human [65]. This current plays an important role in shaping the photoreceptor light response by increasing the transientness of the response, an effect similar to that of a high-pass filter [41].…”

“…This current plays an important role in shaping the photoreceptor light response by increasing the transientness of the response, an effect similar to that of a high-pass filter [41]. It is also implicated in the adaptation of cones to contrast when processing natural scenes [63].…”

Rod signaling in primate retina: range, routing and kinetics

“…Recent work on current-to-voltage transformations in mouse and goldfish photoreceptors indicates that intrinsic conductances can speed visual responses in rods and cones (Sothilingam et al, 2016; Seeliger et al, 2011; Della Santina et al, 2012; Howlett, Smith, & Kamermans, 2017). Could a similar mechanism account for the additional speeding between rod outer segment currents and RGC responses?…”

“…Specifically, we find that the speeding of rod signals in the retinal output can be explained by a change in kinetics of signals in the rods themselves - with approximately equal contributions from phototransduction and inner segment conductances. Inner segment conductances similarly speed responses of mouse rods and goldfish cones (Sothilingam et al, 2016; Seeliger et al, 2011; Della Santina et al, 2012; Howlett et al, 2017).…”