A novel mechanism of cone photoreceptor adaptation

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.Author summary: An animal’s ability to survive depends on its ability to adapt to a wide range of light conditions, by maximizing the information flow through the retina. Here, we show a new form of adaptation in cone photoreceptors that helps them optimize the information they transmit by adjusting their response kinetics to better match the visual conditions. The adaptive mechanism we describe is independent of the cone phototransduction process and is instead mediated by membrane processes in which the hyperpolarization-activated current, Ih, plays a critical role. Consistent with the critical role of this current, we also found that cones sensitive to short wavelengths lacked a prominent Ih current and did not show this new form of adaptation. As voltage-dependent processes underlie the adaptational mechanism, it is only apparent when the stimuli are able to sufficiently modulate the membrane potential of cones. This happens with natural stimuli, which are able to deliver high levels of “effective” contrast. However, even though this new adaptive mechanism can be driven by contrast, we argue in the Discussion that in its strictest sense it is not a contrast adaptation mechanism per se.