Thresholds and noise limitations of colour vision in dim light

Colour discrimination is based on opponent photoreceptor interactions, and limited by receptor noise. In dim light, photon shot noise impairs colour vision, and in vertebrates, the absolute threshold of colour vision is set by dark noise in cones. Nocturnal insects (e.g. moths and nocturnal bees) and vertebrates lacking rods (geckos) have adaptations to reduce receptor noise and use chromatic vision even in very dim light. In contrast, vertebrates with duplex retinae use colour-blind rod vision when noisy cone signals become unreliable, and their transition from cone- to rod-based vision is marked by the Purkinje shift. Rod–cone interactions have not been shown to improve colour vision in dim light, but may contribute to colour vision in mesopic light intensities. Frogs and toads that have two types of rods use opponent signals from these rods to control phototaxis even at their visual threshold. However, for tasks such as prey or mate choice, their colour discrimination abilities fail at brighter light intensities, similar to other vertebrates, probably limited by the dark noise in cones. This article is part of the themed issue 'Vision in dim light’.

The electroretinogram of the rhodopsin knockout mouse

The electroretinogram (ERG) of the rhodopsin knockout (rho−/−) mouse of Humphries et al. (1997) (Humphries et al., 1997) was studied for evidence of light-evoked rod activity and to describe the cone function. The rho−/− retina develops normal numbers of rod and cone nuclei, but the rods have no outer segments, and no rhodopsin is found by immunohistochemistry. The dark-adapted ERG threshold was elevated 4.7 log units above wild-type (WT) control mice, indicating that any residual rod responses were reduced >50,000-fold, consistent with a complete functional knockout. The dark-adapted rho−/− ERG had a cone waveform, and the spectral sensitivity peaked near 510 nm for both dark-adapted and light-adapted conditions, without evidence of a Purkinje shift. The light-adapted ERG b-wave amplitude of young rho−/− mice was the same as WT. The amplitude remained steady up to postnatal day P47, but thereafter it declined to only 1–2% by P80 when no cone outer segments remained. Cone b-wave threshold of dark-adapted rho−/− mice was −1.07 ± 0.39 log cd-s/m2 (n = 17), which is 1.27 log units more sensitive than light-adapted thresholds against a rod-suppressing Ganzfeld background of 1.61 log scotopic cd/m2. This indicates that dark-adapted WT responses to still dimmer stimuli are exclusively rod driven with minimal cone intrusion. Above this cone threshold intensity, the dark-adapted b-wave of WT will be a summation of rod and cone responses. Threshold versus intensity (TVI) studies gave no evidence of a rod influence on the mouse cone b-wave.

Photic Environment, Visual Pigments, and the Limits of the Visible Spectrum

The limits of the visible spectrum are set by the light available for vision, and by the visual pigment absorbance. The hundreds of visual pigments studied to the present day have absorbance maxima spread within the range from 350 to 620 nm. Yet this diversity is used for vision quite nonuniformly: rod and cone visual pigments are tightly clustered around a few preferred positions in the spectrum, eg near 500 nm in the rods of land animals. The so-called ‘sensitivity hypothesis’ assumes that the clustering is to maximise the number of absorbed photons available in the animals' light environment. In most cases, however, visual pigments are substantially more short-wave (blue-shifted) than is necessary for maximum quantal absorption. Examples of the ‘blue shift’ are the Purkinje shift during cone - rod transition in dark adaptation, the hypsochromic shift of rod visual pigments in deep-water fish, and a similar shift in the cone pigments of geckos and some snakes as a result of evolutionary adaptation to nocturnal habits. It is argued that an important limiting factor in vision is the dark noise produced by thermal isomerisation of the chromophore. Measurements of the dark noise in rods with different visual pigments show that the noise increases steeply when the absorbance maximum is shifted to longer wavelengths, thus precluding the use of long-wave pigments for vision at low intensities. The optimum spectral position of a pigment may be that which ensures a maximum light-to-noise ratio in a particular photic environment.

Depletion of retinal dopamine does not affect the ERG b-wave increment threshold function in goldfish in vivo

Increment threshold functions of the electroretinogram (ERG) b–wave were obtained from goldfish using an in vivo preparation to study intraretinal mechanisms underlying the increase in perceived brightness induced by depletion of retinal dopamine by 6–hydroxydopamine (6–OHDA). Goldfish received unilateral intraocular injections of 6–OHDA plus pargyline on successive days. Depletion of retinal dopamine was confirmed by the absence of tyrosine-hydroxylase immunoreactivity at 2 to 3 weeks postinjection as compared to sham-injected eyes from the same fish. There was no difference among normal, sham-injected or 6–OHDA-injected eyes with regard to ERG waveform, intensity-response functions or increment threshold functions. Dopamine-depleted eyes showed a Purkinje shift, that is, a transition from rod-to-cone dominated vision with increasing levels of adaptation. We conclude (1) dopamine-depleted eyes are capable of photopic vision; and (2) the ERG b–wave is not diagnostic for luminosity coding at photopic backgrounds. We also predict that (1) dopamine is not required for the transition from scotopic to photopic vision in goldfish; (2) the ERG b–wave in goldfish is influenced by chromatic interactions; (3) horizontal cell spinules, though correlated with photopic mechanisms in the fish retina, are not necessary for the transition from scotopic to photopic vision; and (4) the OFF pathway, not the ON pathway, is involved in the action of dopamine on luminosity coding in the retina.

Performance of Genetically-Colorblind Individuals on a Rapid Dark Adaptation Test Based on the Purkinje Shift

An experiment was conducted to determine whether or not genetic colorblindness would limit performance on a rapid dark adaptation test (RDAT) which is based on the Purkinje shift in retinal sensitivity to lower wavelengths of light energy under mesopic/scotopic conditions of illumination. No differences in RDAT performance between age-equivalent colorblind and non-colorblind subjects was observed.