Rods progressively escape saturation to drive visual responses in daylight conditions

Abstract

Rod and cone photoreceptors support vision across large light intensity ranges. Rods, active under dim illumination, are thought to saturate at higher (photopic) irradiances. The extent of rod saturation is not well defined; some studies report rod activity well into the photopic range. Using electrophysiological recordings from retina and dorsal lateral geniculate nucleus of cone-deficient and visually intact mice, we describe stimulus and physiological factors that influence photopic rod-driven responses. We find that rod contrast sensitivity is initially strongly reduced at high irradiances, but progressively recovers to allow responses to moderate contrast stimuli. Surprisingly, rods recover faster at higher light levels. A model of rod phototransduction suggests that phototransduction gain adjustments and bleaching adaptation underlie rod recovery. Consistently, exogenous chromophore reduces rod responses at bright background. Thus, bleaching adaptation renders mouse rods responsive to modest contrast at any irradiance. Paradoxically, raising irradiance across the photopic range increases the robustness of rod responses.

Neural circuits in the mouse retina support color vision in the upper visual field

“…This is consistent with a recent study showing that color-opponent responses of ventral JAM-B RGCs originate from a rod-cone opponent mechanism involving HCs (Joesch and Meister, 2016) . The prerequisites for this rod-mediated mechanism have been experimentally established: First, mouse rods can drive visual responses at the low photopic light levels used in our experiments (Tikidji-Hamburyan et al, 2017) and, second, rod signals travel in HCs from the axon terminals to the soma via the HC axon ( (Szikra et al, 2014) ; but see (Trümpler et al, 2008) ).…”

“…This arrangement might also be relevant in other species with a regional increase in S-opsin density in their retina (reviewed in (Peichl, 2005) ), including the common shrew (Peichl et al, 2000) or some hyenas (Calderone et al, 2003) . Because mouse rod photoreceptors are active in the photopic regime (Tikidji-Hamburyan et al, 2017) , rod-cone opponency likely contributes to the animal's color vision across a substantial intensity range, increasing its relevance for informing behavior.…”

Pulses of melanopsin-directed contrast produce highly reproducible pupilresponses that are insensitive to a change in background radiance

“…Because the stimulus background is in the photopic range, we generally assume that the rods are saturated, and thus this rod contrast does not contribute to the observed pupil response. This assumption, however, may be challenged by recent work that finds rods can signal above their nominal saturation threshold 48 . It is therefore reassuring to observe in the current study that the pupil response is unchanged with the increased stimulus intensity used in Session 3.…”

Regulation of calcium homeostasis in the outer segments of rod and cone photoreceptors

“…Yet, rods are able to detect single photons in darkness and function up to ambient light levels producing ~10 5 R* rod −1 s −1 corresponding to natural scenes from cloudy moonless night to about sunrise (Aguilar and Stiles, 1954; Hess et al, 1989; Naarendorp et al, 2010; Sharpe et al, 1992; Sharpe and Nordby, 1990) (but see also (Tikidji-Hamburyan et al, 2017)). The functional range of cones is even wider and they are able to detect light from starry night to bright sunny day (Boynton and Whitten, 1970; Naarendorp et al, 2010; Stiles, 1939; Valeton and van Norren, 1983).…”

“…Rods saturate under moderately bright light and are mostly unable to mediate vision in bright daytime conditions (Figure 3) (Baylor et al, 1984; Thomas and Lamb, 1999) but see (Tikidji-Hamburyan et al, 2017)). In contrast, cones are able to respond to light of practically any natural illumination level that exists on Earth or under experimental conditions (Burkhardt, 1994; Jones et al, 1993; Schnapf et al, 1990).…”