Visual and circadian responses to light in aged retinally degenerate mice

Provencio, Ignacio; Wong, S.W.; Lederman, Andrew; Argamaso, Sharleen M.; Foster, Russell G.

doi:10.1016/0042-6989(94)90304-2

Cited by 122 publications

(60 citation statements)

References 29 publications

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“…This possibility is consistent with the finding that naturally occurring and transgenic mice that lack rods and cones, although maintaining an apparently normal inner retina, are capable of photoregulating circadian locomotor activity rhythms and pineal melatonin levels in a manner indistinguishable from wild-type controls (Foster et al, 1991;Provencio et al, 1994;Freedman et al, 1999). Bilateral removal of the eyes abolishes such regulation (Nelson and Zucker, 1981).…”

Section: Discussionsupporting

confidence: 76%

A Novel Human Opsin in the Inner Retina

et al. 2000

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Here we report the identification of a novel human opsin, melanopsin, that is expressed in cells of the mammalian inner retina. The human melanopsin gene consists of 10 exons and is mapped to chromosome 10q22. This chromosomal localization and gene structure differs significantly from that of other human opsins that typically have four to seven exons. A survey of 26 anatomical sites indicates that, in humans, melanopsin is expressed only in the eye. In situ hybridization histochemistry shows that melanopsin expression is restricted to cells within the ganglion and amacrine cell layers of the primate and murine retinas. Notably, expression is not observed in retinal photoreceptor cells, the opsin-containing cells of the outer retina that initiate vision. The unique inner retinal localization of melanopsin suggests that it is not involved in image formation but rather may mediate nonvisual photoreceptive tasks, such as the regulation of circadian rhythms and the acute suppression of pineal melatonin. The anatomical distribution of melanopsinpositive retinal cells is similar to the pattern of cells known to project from the retina to the suprachiasmatic nuclei of the hypothalamus, a primary circadian pacemaker.

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Section: Discussionsupporting

confidence: 76%

A Novel Human Opsin in the Inner Retina

et al. 2000

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“…3 and 4). A primacy of rod-cone input during conditioned responses is supported by previous work showing that rodless-coneless mice show deficits [rd/rd cl strain (12)] or are unresponsive [Pde6b rd1/rd1 strain (13)] to light as a conditioned stimulus in a learned avoidance task.…”

Section: Discussionsupporting

confidence: 56%

Light enhances learned fear

Warthen¹,

Wiltgen

Provencio³

2011

Proc. Natl. Acad. Sci. U.S.A.

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The ability to learn, remember, and respond to emotional events is a powerful survival strategy. However, dysregulated behavioral and physiological responses to these memories are maladaptive. To fully understand learned fear and the pathologies that arise during response malfunction we must reveal the environmental variables that influence learned fear responses. Light, a ubiquitous environmental feature, modulates cognition and anxiety. We hypothesized that light modulates responses to learned fear. Using tone-cued fear conditioning, we found that light enhances behavioral responses to learned fear in C57BL/6J mice. Mice in light freeze more in response to a conditioned cue than mice in darkness. The absence of significant freezing during a 2-wk habituation period and during intertrial intervals indicated that light specifically modulates freezing to the learned acoustic cue rather than the context of the experimental chamber. Repeating our assay in two photoreceptor mutant models, Pde6b rd1/rd1 and Opn4 −/− mice, revealed that lightdependent enhancement of conditioned fear is driven primarily by the rods and/or cones. By repeating our protocol with an altered lighting regimen, we found that lighting conditions acutely modulate responses when altered between conditioning and testing. This is manifested either as an enhancement of freezing when light is added during testing or as a depression of freezing when light is removed during testing. Acute enhancement, but not depression, requires both rod/cone-and melanopsin-dependent photoreception. Our results demonstrate a modulation by light of behavioral responses to learned fear.L ight is a pervasive feature of the environment and exerts broad effects on behavior and physiology via two parallel pathways (1). The familiar image-forming visual pathway allows discernment of objects in the environment according to physical qualities: their color, form, texture, and motion. The parallel non-image forming (NIF) pathway enables light to exert numerous effects on physiology and behavior independently of image formation, such as pupil constriction, modulation of heart rate, and the synchronization of circadian rhythms and sleepwake cycles to the daily light-dark cycle (2). In addition to the effects of light on basic physiological functions, light also modulates higher-order cognitive processes, including anxiety, mood, and alertness/awakeness (3, 4). The retina, the sole photosensory organ in mammals, projects directly to brain regions involved in emotional responses. Among these are the amygdala, the bed nucleus of the stria terminalis, and the periaqueductal gray (5). Activity in some of these regions is known to be acutely modulated by light in a wavelength-dependent manner (3, 6), whereas the link between photoreception and function in other retinorecipient emotional processing areas remains to be elucidated.Brain sites involved in emotional processing participate in the critical function of learning and remembering emotionally arousing events. This function enables ...

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“…are not necessary for transmission of light information to the circadian clock in the suprachiasmatic nucleus (3,5). Two families of candidate photoreceptors have been proposed to function in the absence of classical ocular photoreceptors to mediate signal transduction of light to the SCN: novel opsins and cryptochromes.…”

Section: Discussion Circadian Photoreceptors In Mammals Extensive Anmentioning

confidence: 99%

“…Although it is well established that the opsin protein family comprises the visual photoreceptors, the classical opsins (rhodopsin and color opsin) are not required for circadian photoreception. Behavioral and in vivo biochemical analyses in retinal degenerate (rd) mice have shown that the outer retina (containing the rod and cone photoreceptors) is not necessary for circadian entrainment by light, suggesting that a pigment located in the inner retina acts as the circadian photoreceptor (2)(3)(4)(5). Three candidate photoreceptive proteins, melanopsin (6) and cryptochromes 1 and 2 (7,8), are primarily expressed in the inner retina.…”

mentioning

confidence: 99%

Preservation of light signaling to the suprachiasmatic nucleus in vitamin A-deficient mice

Thompson

Blaner

Gelder

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

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To investigate the role of retinal-based pigments (opsins) in circadian photoreception in mice, animals mutated in plasma retinol binding protein were placed on a vitamin A-free diet and tested for photic induction of gene expression in the suprachiasmatic nucleus. After 10 months on the vitamin A-free diet, the majority of mice contained no detectable retinal in their eyes. These mice demonstrated fully intact photic signaling to the suprachiasmatic nucleus as measured by acute mPer mRNA induction in the suprachiasmatic nucleus in response to bright or dim light. The data suggest that a non-opsin pigment is the primary circadian photoreceptor in the mouse.circadian photoreceptor ͉ retinol binding protein

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Visual and circadian responses to light in aged retinally degenerate mice

Cited by 122 publications

References 29 publications

A Novel Human Opsin in the Inner Retina

A Novel Human Opsin in the Inner Retina

Light enhances learned fear

Preservation of light signaling to the suprachiasmatic nucleus in vitamin A-deficient mice

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