Rod Phototransduction Determines the Trade-Off of Temporal Integration and Speed of Vision in Dark-Adapted Toads

Abstract

Human vision is ϳ10 times less sensitive than toad vision on a cool night. Here, we investigate (1) how far differences in the capacity for temporal integration underlie such differences in sensitivity and (2) whether the response kinetics of the rod photoreceptors can explain temporal integration at the behavioral level. The toad was studied as a model that allows experimentation at different body temperatures. Sensitivity, integration time, and temporal accuracy of vision were measured psychophysically by recording snapping at worm dummies moving at different velocities. Rod photoresponses were studied by ERG recording across the isolated retina. In both types of experiments, the general timescale of vision was varied by using two temperatures, 15 and 25°C. Behavioral integration times were 4.3 s at 15°C and 0.9 s at 25°C, and rod integration times were 4.2-4.3 s at 15°C and 1.0 -1.3 s at 25°C. Maximal behavioral sensitivity was fivefold lower at 25°C than at 15°C, which can be accounted for by inability of the "warm" toads to integrate light over longer times than the rods. However, the long integration time at 15°C, allowing high sensitivity, degraded the accuracy of snapping toward quickly moving worms. We conclude that temporal integration explains a considerable part of all variation in absolute visual sensitivity. The strong correlation between rods and behavior suggests that the integration time of dark-adapted vision is set by rod phototransduction at the input to the visual system. This implies that there is an inexorable trade-off between temporal integration and resolution.

The photovoltage of rods and cones in the dark‐adapted mouse retina

“…An average unperturbed TTP of rods at 36°C of 147 ms falls in the middle of previously reported values for mammalian rods at body temperature (macaque/patch: 200–218 ms in Schneeweis & Schnapf, 1995, 2000; macaque/suction pipette: 190 ms in Baylor et al 1984; human/suction pipette: 189 ms in Kraft et al 1993; mouse/suction pipette: 104 ms in Burns et al 2002; 180 ms in Nikonov et al 2005, 2006; 218 ms in Dunn et al 2006; 181 in Azevedo & Rieke, 2011; mouse, rat/ in vitro ERG: 150 in Nymark et al 2005; 120–130 in Vinberg et al 2009). There is significant divergence in the literature regarding cone kinetics (reviewed in Haldin et al 2009), but recent suction pipette (Nikonov et al 2006) and in vitro ERG recordings (Heikkinen et al 2008) reported a TTP of ∼50 ms for mouse cones at body temperature, in line with our present estimate with patch clamp. It must be noted that the possible presence of a gap junction‐mediated rod component in our cone recordings (see below) may have influenced our measurements of cone TTP.…”

Photoreceptors and eyes of pikeperch Sander lucioperca, pike Esox lucius, perch Perca fluviatilis and roach Rutilus rutilus from a clear and a brown lake

“…Given the slow response kinetics of vertebrate rods at low temperatures (Nymark et al, 2005), the visual latency of species A may be shorter by several seconds compared with that of species B (cf. Aho et al, 1993;Haldin et al, 2009).…”

Flicker-induced eye movements and the behavioural temporal cut-off frequency in a nocturnal spider

“…The neural images in the toads' eyes and the spiders' motionless secondary eyes are assumed to adapt to stationary surroundings, and only moving objects would pop up on the animals' retinae (Ewert and Borchers, 1974;Land and Barth, 1992). Toad rod photoreceptor cells have integration times of 1.0-1.3s at 25°C, and substantially longer integration times at lower temperatures (Haldin et al, 2009) and are thus roughly 10 times slower than photoreceptors in C. salei. A good match was found between the integration time of the toad rod photoreceptor cells at different temperatures and the 'exposure time' of a dummy necessary to elicit prey capture (Haldin et al, 2009).…”

“…Toad rod photoreceptor cells have integration times of 1.0-1.3s at 25°C, and substantially longer integration times at lower temperatures (Haldin et al, 2009) and are thus roughly 10 times slower than photoreceptors in C. salei. A good match was found between the integration time of the toad rod photoreceptor cells at different temperatures and the 'exposure time' of a dummy necessary to elicit prey capture (Haldin et al, 2009).…”

“…In these experiments, no directional information has to be taken into account by the animals, in contrast to studies based on optomotor response or prey capture (e.g. Autrum and Stoecker, 1950;Autrum, 1952;Haldin et al, 2009) where the animals have to compute the direction of moving stimuli. Nor are the animals required to learn, as is the case in studies based on discrimination tasks (e.g.…”