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Molecular Basis of Dark Adaptation in Rod Photoreceptors

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Molecular Basis of Dark Adaptation in Rod Photoreceptors 1 Molecular basis of dark c.s. LEIBROCK , T. REUTER, T.D. LAMB adaptation in rod photoreceptors Abstract visual threshold (logarithmically) against time, following 'bleaching' exposures of different Following exposure of the eye to an intense strengths. After an almost total bleach light that 'bleaches' a significant fraction of (uppermost trace) the visual threshold recovers the rhodopsin, one's visual threshold is along the classical bi-phasic curve: the initial initially greatly elevated, and takes tens of rapid recovery is due to cones, and the second minutes to recover to normal. The elevation of slower component occurs when the rod visual threshold arises from events occurring threshold drops below the cone threshold. within the rod photoreceptors, and the (Note that in this old work, the term 'photon' underlying molecular basis of these events was used for the unit now defined as the and of the rod's recovery is now becoming troland; x trolands is the illuminance at the clearer. Results obtained by exposing isolated retina when a light of 1 cd/m2 enters a pupil toad rods to hydroxylamine solution indicate with cross-sectional area x mm2.) that, following small bleaches, the primary intermediate causing elevation of visual threshold is metarhodopsin II, in its Questions and observations phosphorylated and arrestin-bound form. This The basic question in dark adaptation, which product activates transduction with an efficacy has not been answered convincingly in the six about 100 times greater than that of opsin. decades since the results of Fig. 1 were obtained, Key words Bleaching, Dark adaptation, is: Why is one not able to see very well during Metarhodopsin, Noise, Photoreceptors, the period following a bleaching exposure? Or, Sensitivity more explicitly: What is the molecular basis for the slow recovery of visual performance during dark adaptation? In considering the answers to these questions, there are three long-standing observations that need to be borne in mind. C.S. Leibrock Introduction T.D. Lamb[2!g (1) Firstly, the desensitisation of the overall The phenomena of light adaptation and Department of Physiology visual system is far in excess of the fraction of University of Cambridge dark adaptation pigment bleached. For example, with a bleach of Downing Street The visual system is able to adapt to a very wide just 4% (the second lowest trace in Fig. 1), visual Cambridge CB2 3EG, UK range of intensities, from starlight levels to threshold is elevated initially by more than Tel: +44 (0)1223 333856 bright sunlight. Under many conditions such 1000-fold (3 log units), and after 1 min of Fax: +44 (0)1223 333840 adaptation occurs very rapidly (within sec­ recovery it remains elevated by more than 100- e-mail: [email protected]. onds), whether the background intensity is fold (2 log units). This shows that the raised T. Reuter increasing or decreasing, and this ability of the threshold cannot have been caused by lack of Department of Ecology and visual system to rapidly alter its adaptational rhodopsin available to absorb light, because in Systematics state is referred to as light adaptation. this case the vast bulk of the pigment (the other Division of Instruction in Swedish The term dark adaptation (synonymous with 96°;(,) was still present. Rather than lack of Zoological Laboratory bleaching adaptation) refers to the special case of photo pigment, it is the presence of a University of Helsinki recovery of the visual system in darkness photoproduct that causes the desensitisation. PB 17, FIN-00014 Helsinki following exposure of the eye to intense (2) Secondly, it is important to realise that Finland illumination that bleaches an appreciable fraction the slowness of recovery of visual sensitivity 1 Present address: (say, more than 0.01%) of the photopigment, can in no way be advantageous to the owner of ZF-FPB Gebaude E41 rhodopsin. Following intense exposures it is the eye, and indeed it must be disadvantageous, Bayer AG found that recovery can be very slow, taking as discussed by Barlow2 and Lamb.3 Thus, if an 51368 Leverkusen many minutes. Indeed, following a total bleach animal (or, perhaps, a caveman) were to enter a Germany (of 100% of the rhodopsin) complete recovery dark cave after having been out on a bright can take as long as 50 min. sunny beach, then there could be no survival Supported by grants from the Wellcome Trust The original dark adaptation results of advantage in being unable to see properly for (034792) and the Human Hecht, Haig and Chase1 obtained more than 60 half-an-hour. In this sense, the term 'adaptation' Frontiers Science Program years ago are illustrated in Fig. 1, which plots is very misleading as a description of the period (RG-62/94) Eye (1998) 12, 511-520 © 1998 Royal College of Ophthalmologists 511 8 Adaptt"nglntensify o 400.,0 00 photons 6 A .3�900 " c " e /1 v " 4 2 o � 20 JO 40 Time in Porlr- l1/nvfes Fig. 1. Classical dark adaptatioll curves for a Ilormal obsCl'l'CI'. Thre,hold for detecti(J/1 of a testflash is plotted 011 a lo;.;aritllmic scale, a;.;aillst time aftt'/' hleachill;';, for bleaches offi"e levels, each of 2 mill duratiol/. Note tlltlt ti,e til/it of retil/al ilitllllil/Illtce, the trolalld, was ill those days termed the 'photoll'. Reproduced u'ith permissioll from Hecht et a1.' following a bleach, as it suggests that the visual system Post-bleach desensitisation and noise in toad rods has been adjusted in this way so as to improve its Recordings from rod photoreceptors have shown that, performance. Instead, the performance of the visual following small bleaches, the rods behave as though they system has been seriously degraded, and during the are experiencing light - they exhibit both desensitisation period of 'dark adaptation' the system slowly recovers and noise, closely similar to the effects of real light. All back to the fully sensitive state that it exhibited before the the subsequent results in this paper were obtained from bleach. rod photoreceptors isolated from the retina of the toad, (3) Thirdly, in considering the underlying basis of Buja lIlarill!lS, and recorded using the suction pipette dark adaptation, it is important to bear in mind the technique." In considering results from amphibian rods, classical observations of Stiles and Crawford: who one needs to bear in mind that responses obtained at showed in 1932 that during the course of dark adaptation room temperature (c. 22°C) are about a factor of 5X the visual system behaves as though the world is being slower than responses obtained at mammalian body viewed through a 'veiling light' that gradually fades temperature, and that adaptational changes are similarly away. In other words Stiles and Crawford found that, slowed down. following a bleach, the visual system behaves as though the eye is experiencing something equivalent to light (which they termed the 'equivalent background Desensitisation intensity') and that during the course of dark adaptation It has long been known that the rod pathway in the retina the intensity of this equivalent background slowly fades becomes desensitised following a bleach,"'? and that the away. recovery of sensitivity proceeds steadily and A primary aim of dark adaptation research is to spontaneously. Dowling" proposed that the early rapid account in molecular terms for the occurrence of this component of recovery represented a fast neural bleach-induced equivalent background. Experiments on adaptation, while the slower recovery (taking tens of isolated rod photoreceptors have demonstrated the minutes to hours) was photochemical and depended on existence of equivalent light at the single-cell level, and the regeneration of rhodopsin. Donner and Reuter,l on have indicated the likely molecular basis of the the other hand, suggested that most of the adaptation phenomenon. was related to processes in the rods themselves, and they 512 presented evidence indicating that the relatively rapid background illumination (see for example Fig. 12 in recovery of sensitivity after small bleaches (3-6%) LambI4). As indicated by the dashed arrow in Fig. 2, depended on the decay of the photochemical backgrounds of increasing intensity similarly cause intermediate metarhodopsin II. progressive decreases in flash sensitivity and The results in Fig. 2 (from Leibrock et al.B) typify the acceleration of the response. Hence, following a bleach, desensitisation and recovery that are seen in an isolated the rod is desensitised in exactly the same way as though rod following very small bleaches (of just under 1% in it were experiencing a background light that slowly this case). The traces plot responses to constant dim test faded away. In a subsequent figure (Fig. 4) we plot the flashes, presented either before the bleach (top trace) or 'desensitisation-equivalent intensity' as a function of at the indicated times (in minutes) after the bleach. time after the bleach. Immediately after the bleach, the response was greatly desensitised and considerably accelerated, but as time Noise progressed the response to the fixed test flash grew steadily larger, and its peak moved later, until after about If a photoreceptor were really experiencing something an hour of dark adaptation the response had returned equivalent to light following a bleach, then it would almost to its pre-bleach level. exhibit increased noise as a result of photon fluctuations, Under physiological conditions, complete recovery (of i.e. as a consequence of the quantal nature of light. Such the kind illustrated in Fig. 2) must be obtained bleach-induced fluctuations are indeed observed,15 as eventually. However, in experiments on rods isolated exemplified by the long recording in Fig. 3. In this from the retinal pigment epithelium (RPE), complete recovery is obtained only in the case of small bleaches, of less than about 5% of the rhodopsin.
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