Entrainment of the circadian activity rhythm to the light cycle: Effective light intensity for a Zeitgeber in the retinal degenerate C3H mouse and the normal C57BL mouse

Ebihara, Shizufumi; Tsuji, Keiichiro

doi:10.1016/0031-9384(80)90246-2

Cited by 104 publications

(81 citation statements)

References 32 publications

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“…These investigators reported that adult rd/rd mice were able to synchronize their circadian activity rhythms to cycles of light and darkness. Similar to Keeler (1927), Ebihara and Tsuji (1980) also suggested that cells other than rods and cones in the retina might be directly light sensitive. However, the universally acknowledged depiction of the organization of the mammalian retina prevailed despite these reports indicating that rodents with severe degeneration of the outer retina remained capable of responding to light (i.e., generating irradiance responses).…”

Section: The Convergence Of Retinal Physiology and Internal Time Keepingsupporting

confidence: 62%

“…However, the threshold of the response was unusually high for the rod-dominated rodent retina and the temporal integration of the stimulus was also unusual for a rod-mediated response (Takahashi et al 1984). Ebihara and Tsuji (1980) and later Foster et al (1991) used rd mice to assess whether rod and/or cone photoreceptors conveyed photoentrainment signals to the SCN. Mice carrying the retinal degeneration mutation (rd; the mutation identified by Keeler 1924), are virtually devoid of rod and cone photoreceptors by four weeks of age and do not produce recordable electroretinographic responses or visual evoked potentials (Farber et al 1994).…”

Section: The Convergence Of Retinal Physiology and Internal Time Keepingmentioning

confidence: 99%

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Intrinsically Photosensitive Retinal Ganglion Cells

Pickard

Sollars

2011

Reviews of Physiology, Biochemistry and Pharmacology 162

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Intrinsically photosensitive retinal ganglion cells (ipRGCs) respond to light in the absence of all rod and cone photoreceptor input. The existence of these ganglion cell photoreceptors, although predicted from observations scattered over many decades, was not established until it was shown that a novel photopigment, melanopsin, was expressed in retinal ganglion cells of rodents and primates. Phototransduction in mammalian ipRGCs more closely resembles that of invertebrate than vertebrate photoreceptors and appears to be mediated by transient receptor potential channels. In the retina, ipRGCs provide excitatory drive to dopaminergic amacrine cells and ipRGCs are coupled to GABAergic amacrine cells via gap junctions. Several subtypes of ipRGC have been identified in rodents based on their morphology, physiology and expression of molecular markers. ipRGCs convey irradiance information centrally via the optic nerve to influence several functions including photoentrainment of the biological clock located in the hypothalamus, the pupillary light reflex, sleep and perhaps some aspects of vision. In addition, ipRGCs may also contribute irradiance signals that interface directly with the autonomic nervous system to regulate rhythmic gene activity in major organs of the body. Here we review the early work that provided the motivation for searching for a new mammalian photoreceptor, the ground-breaking discoveries, current progress that continues to reveal the unusual properties of these neuron photoreceptors, and directions for future investigation.Keywords: Melanopsin, Circadian rhythms, Suprachiasmatic nucleus, Retina digitalcommons.unl.edu P i c k a r d & S o l l a r S i n R e v P h y s i o l B i o c h e m P h a R m a c o l1 6 2 ( 2 0 1 2 ) Early Hints of a Third Photoreceptor in the Mammalian RetinaThe perception of shapes, color and objects moving in the world begins in the outer retina where light is absorbed by photopigments that are integral membrane apoproteins (opsins) covalently linked to a retinaldehyde chromophore in the rod and cone photoreceptors. The capturing of photons by rod and cone photoreceptors initiates a signaling cascade in which photon capture is converted into an electrical signal. The simplest common pathway these signals take from the eye to the brain is from the photoreceptors to bipolar cells to ganglion cells. Retinal ganglion cells (RGCs) convey the signals centrally as action potentials, transmitted via their axons in the optic nerve, to higher brain regions for integration and the further processing required for conscious visual perception (Fig. 1). Among non-mammalian vertebrates, photoreceptors are also found in locations outside the retina, including the pineal gland and in the brain itself. These extra-ocular photoreceptors mediate tasks not associated directly with visual perception (non-image forming functions such as hormone regulation). However, since the pioneering descriptions of the vertebrate retina by Santiago Ramón y Cajal in the late 1800s, it was believed that t...

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Section: The Convergence Of Retinal Physiology and Internal Time Keepingsupporting

confidence: 62%

Section: The Convergence Of Retinal Physiology and Internal Time Keepingmentioning

confidence: 99%

Intrinsically Photosensitive Retinal Ganglion Cells

Pickard

Sollars

2011

Reviews of Physiology, Biochemistry and Pharmacology 162

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“…It is nevertheless premature to discount a potential contribution from rods at lower light levels. At scotopic levels, Aggelopoulos and Meissl (2000) report a roddominated response in SCN neurons with a peak spectral sensitivity at 505 nm that shifts to 510 nm [mid-wavelength (MW) opsin] in photopic conditions, and rods appear to be required for entrainment at low light levels (Ebihara and Tsuji, 1980;Mrosovsky, 2003) Cone (and rod) signals from the outer retina can be relayed to the SCN via pathways from melanopsin ipRGCs or nonmelanopsin RGCs (Morin et al, 2003;Sollars et al, 2003;Hattar et al, 2006). The ON-OFF responses are derived from the well known anatomical and physiological stratification of the inner plexiform layer (Wassle, 2004).…”

Section: Discussionmentioning

confidence: 99%

“…Mice lacking melanopsin (Panda et al, 2002;Hattar et al, 2003;Panda et al, 2003), cones, or both rods and cones (Freedman et al, 1999;Semo et al, 2003;DkhissiBenyahya et al, 2007) entrain normally to a bright white light/ dark cycle, but exhibit diminished phase shifts to monochromatic stimulations depending on the wavelength and duration of the light pulse. Mice that predominantly lack rods (retinal degeneration; retinal degeneration slow) have normal phase shifts but fail to entrain at low (Ͻ1 lux) light levels (Ebihara and Tsuji, 1980;Mrosovsky, 2003) These different behavioral consequences could be interpreted to reflect a simple complementarity, with the functional loss of one photopigment compensated by the remaining photopigment(s). Although this view is consistent with the coding of different light stimulus attributes by each photoreceptor type (Dacey et al, 2005;Dkhissi-Benyahya et al, 2007), previous in vitro recordings of ipRGCs reveal a greater range of complexity.…”

Section: Introductionmentioning

confidence: 99%

Responses of Suprachiasmatic Nucleus Neurons to Light and Dark Adaptation: Relative Contributions of Melanopsin and Rod–Cone Inputs

Drouyer¹,

Rieux²,

Hut³

et al. 2007

J. Neurosci.

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“…M ice blind from outer retinal degeneration retain the ability to entrain their circadian rhythms to external light-dark cycles, have active pupillary light responses (PLRs), and exhibit photically induced melatonin suppression (1)(2)(3)(4). These responses depend on the opsin family member melanopsin (5), which is expressed exclusively in a subset of intrinsically photosensitive retinal ganglion cells (ipRGCs) (6)(7)(8).…”

mentioning

confidence: 99%

Inner retinal photoreception independent of the visual retinoid cycle

Tu¹,

Owens²,

Anderson³

et al. 2006

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

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Mice lacking the visual cycle enzymes RPE65 or lecithin-retinol acyl transferase (Lrat) have pupillary light responses (PLR) that are less sensitive than those of mice with outer retinal degeneration (rd͞rd or rdta). Inner retinal photoresponses are mediated by melanopsinexpressing, intrinsically photosensitive retinal ganglion cells (ipRGCs), suggesting that the melanopsin-dependent photocycle utilizes RPE65 and Lrat. To test this hypothesis, we generated rpe65 ؊/؊ ; rdta and lrat ؊/؊ ; rd͞rd mutant mice. Unexpectedly, both rpe65 ؊/؊ ; rdta and lrat ؊/؊ ; rd͞rd mice demonstrate paradoxically increased PLR photosensitivity compared with mice mutant in visual cycle enzymes alone. Acute pharmacologic inhibition of the visual cycle of melanopsin-deficient mice with all-trans-retinylamine results in a near-total loss of PLR sensitivity, whereas treatment of rd͞rd mice has no effect, demonstrating that the inner retina does not require the visual cycle. Treatment of rpe65 ؊/؊ ; rdta with 9-cis-retinal partially restores PLR sensitivity. Photic sensitivity in P8 rpe65 ؊/؊ and lrat ؊/؊ ipRGCs is intact as measured by ex vivo multielectrode array recording. These results demonstrate that the melanopsin-dependent ipRGC photocycle is independent of the visual retinoid cycle.melanopsin ͉ pupillary light response ͉ retinal degeneration ͉ retinal ganglion cell ͉ visual photocycle M ice blind from outer retinal degeneration retain the ability to entrain their circadian rhythms to external light-dark cycles, have active pupillary light responses (PLRs), and exhibit photically induced melatonin suppression (1-4). These responses depend on the opsin family member melanopsin (5), which is expressed exclusively in a subset of intrinsically photosensitive retinal ganglion cells (ipRGCs) (6-8). Mice with nonfunctional or degenerated rods and cones that also lack melanopsin show no photically influenced behavior or physiology (9, 10), and intrinsic photosensitivity of retinal ganglion cells is lost in the absence of melanopsin (9,11,12). Melanopsin forms a functional photopigment when heterologously expressed in COS cells (13), Xenopus oocytes (14), Neuro-2A cells (15), or HEK-293 cells (16). Melanopsin is thus necessary for ipRGC photoreception, and is sufficient to confer photosensitivity on intrinsically insensitive cell types. Taken together, these results strongly suggest that melanopsin is the photopigment of inner retinal photoreception.All opsin photopigments use a retinoid chromophore that undergoes isomerization upon absorption of an appropriate wavelength photon. In rod photoreceptors, 11-cis-retinal chromophore is photoisomerized to all-trans-retinal which dissociates from the opsin protein (17). This all-trans-retinal photoproduct is recycled to the active (11-cis) form by enzymatic conversion in the adjacent retinal pigment epithelium (RPE) (18). The chromophore used by melanopsin in situ is not presently known. ipRGCs are physically distant from the enzymatic chromophore regeneration machinery of the RPE. It is present...

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Entrainment of the circadian activity rhythm to the light cycle: Effective light intensity for a Zeitgeber in the retinal degenerate C3H mouse and the normal C57BL mouse

Cited by 104 publications

References 32 publications

Intrinsically Photosensitive Retinal Ganglion Cells

Intrinsically Photosensitive Retinal Ganglion Cells

Responses of Suprachiasmatic Nucleus Neurons to Light and Dark Adaptation: Relative Contributions of Melanopsin and Rod–Cone Inputs

Inner retinal photoreception independent of the visual retinoid cycle

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