The Primary Visual Pathway in Humans Is Regulated According to Long-Term Light Exposure through the Action of a Nonclassical Photopigment light levels. Among the features of this transition are (1) a nocturnal reduction in the threshold for rod-driven responses and scotopic sensitivity [1, 2], (2) a diurnal variation in chromatic sensitivity [3], and (3) a nocturnal decrease in the speed with which signals originating in

  • Hankins M
  • Lucas R
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Abstract

cone photoreceptors are processed [4]. The primary transition between scotopic and photopic Fulham Palace Road London W6 8RF vision (the switch from employing rod to cone photore-ceptors) is a direct response to environmental irradi-United Kingdom ance. However, many events associated with this transi-tion are longer-term adaptations driven by endogenous circadian clocks and/or assessments of light history Summary over time periods of tens to hundreds of minutes. One of the most recently identified of these adaptations illus-Background: The mammalian eye shows marked adap-trates this point. Under natural ambient light cycles, the tations to time of day. Some of these modifications are response of retinal second-order neurones to stimula-not acute responses to short-term light exposure but tion by cone photoreceptors is significantly slower at rely upon assessments of the photic environment made night than during the day. The function of this adaptation over several hours. In the past, all attempts at a mecha-may be to overcome the temporal disparity in the re-nistic understanding have assumed that these adapta-sponse of rods and cones under light levels when both tions originate with light detection by one or other of the will be active [4]. The role of retinal and/or hypothalamic classical photoreceptor cells (rods or cones). However, circadian clocks in generating this rhythm remains un-previous work has demonstrated that the mammalian certain. However, a primary determinant appears to be eye contains non-rod, non-cone photoreceptors. This long-term retinal light exposure. Thus, light delivered at study aimed to determine whether such photoreceptors night will shift the cone pathway toward the daytime contribute to retinal adaptation. state, while darkness during the day has the opposite effect. Results: In the human retina, second-order processing In the laboratory or clinic, this diurnal variation in the of signals originating in cones takes significantly longer cone pathway may be observed using the cone electro-at night than during the day. Long-term light exposure retinogram (ERG). In this approach, external electrodes at night is capable of reversing this effect. Here, we are used to assess electrophysiological field potential employed the cone ERG as a tool to examine the proper-responses of the retina to a brief flash of light (Figure ties of the irradiance measurement pathway driving this 1). It is possible to identify both the initial hyperpolarizing reversal. Our findings indicate that this pathway (1) inte-response of the photoreceptor cells (known as the a grates irradiance measures over time periods ranging wave) and the depolarizing response of second-order from at least 15 to 120 min; (2) responds to relatively neurones initiated by the ON-bipolar cells (b wave) from bright light, having a dynamic range almost entirely out-the ERG (Figure 1) [5]. Under stimuli of sufficient inten-side the sensitivity of rods; (3) acts on the cone pathway sity, the ERG reflects the activity of both rod and cone primarily through a local retinal mechanism; and (4) de-photoreceptors. However, using a background irradi-tects light via an opsin:vitamin A photopigment (␭ max Ϸ ance of light sufficient to saturate rod photoreceptors, 483 nm). it is possible to examine the cone pathway in isolation. Descriptions of the amplitude and timing of the a and Conclusions: A photopigment with a spectral sensitiv-b waves in this cone ERG allow an assessment of the ity profile quite different from those of the classical rod response of cone photoreceptors and cone-driven sec-and cone opsins but matching the standard profile of ond-order neurones. The time taken for the b wave to an opsin:vitamin A-based pigment drives adaptations reach a peak (implicit time) is a benchmark clinical indi-of the human primary cone visual pathway according cator of second-order processing in the retina. The diur-to time of day. nal variation in the processing of cone signals by sec-ond-order neurones is thus observed as a 20% increase Introduction in b wave-implicit time in the middle of the night com-pared to daytime [4]. Similarly, its response to long-term Organisms respond to changes in environmental de-light exposure at night is reflected in a marked decrease mands over the astronomical day in a variety of ways. in implicit time. Some of the most marked adaptations are seen in the Attempts to understand such long-term light adapta-primary visual pathways. The mammalian visual system tions in the mammalian visual system have previously undergoes a complex diurnal transition between pro-assumed they originate with light detection by rod cesses optimized for high (photopic) and low (scotopic) and/or cone photoreceptors. However, there is growing evidence that the mammalian retina contains nonclassi-cal photoreceptors, distinct from the rods and cones, 3 Correspondence: m.hankins@ic.ac.uk

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Hankins, M. W., & Lucas, R. J. (2002). The Primary Visual Pathway in Humans Is Regulated According to Long-Term Light Exposure through the Action of a Nonclassical Photopigment light levels. Among the features of this transition are (1) a nocturnal reduction in the threshold for rod-driven responses and scotopic sensitivity [1, 2], (2) a diurnal variation in chromatic sensitivity [3], and (3) a nocturnal decrease in the speed with which signals originating in. Current Biology, 12, 191–198.

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