Modeling the Role of Mid-Wavelength Cones in Circadian Responses to Light

Nonvisual responses to light, such as photic entrainment of the circadian clock, involve intrinsically light-sensitive melanopsin-expressing ganglion cells as well as rod and cone photoreceptors. However, previous studies have been unable to demonstrate a specific contribution of cones in the photic control of circadian responses to light. Using a mouse model that specifically lacks mid-wavelength (MW) cones we show that these photoreceptors play a significant role in light entrainment and in phase shifting of the circadian oscillator. The contribution of MW cones is mainly observed for light exposures of short duration and toward the longer wavelength region of the spectrum, consistent with the known properties of this opsin. Modeling the contributions of the various photoreceptors stresses the importance of considering the particular spectral, temporal, and irradiance response domains of the photopigments when assessing their role and contribution in circadian responses to light.

[1]  J. Takahashi,et al.  Spectral sensitivity of a novel photoreceptive system mediating entrainment of mammalian circadian rhythms , 1984, Nature.

[2]  J. Heckenlively,et al.  Symposium-in-Print: Photoreceptors Scotopic and Photopic Visual Thresholds and Spatial and Temporal Discrimination Evaluated by Behavior of Mice in a Water Mazet , 2006 .

[3]  S. Roberts.  Transcriptional regulation by WT1 in development. , 2005, Current opinion in genetics & development.

[4]  Á. Szél,et al.  Monoclonal antibody-recognizing cone visual pigment. , 1986, Experimental eye research.

[5]  T. Yoshimura,et al.  Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+) mice , 1996, Journal of Comparative Physiology A.

[6]  J. Hurley,et al.  A thyroid hormone receptor that is required for the development of green cone photoreceptors , 2001, Nature Genetics.

[7]  Satchidananda Panda,et al.  Melanopsin Is Required for Non-Image-Forming Photic Responses in Blind Mice , 2003, Science.

[8]  D. Forrest,et al.  Neurodevelopmental control by thyroid hormone receptors , 2002, Current Opinion in Neurobiology.

[9]  M. Menaker,et al.  Circadian photoreception in the retinally degenerate mouse (rd/rd) , 1991, Journal of Comparative Physiology A.

[10]  Serge Daan,et al.  A functional analysis of circadian pacemakers in nocturnal rodents , 2005, Journal of comparative physiology.

[11]  T. Lamb,et al.  Photoreceptor spectral sensitivities: Common shape in the long-wavelength region , 1995, Vision Research.

[12]  K. Yau,et al.  Diminished Pupillary Light Reflex at High Irradiances in Melanopsin-Knockout Mice , 2003, Science.

[13]  J. Pokorny,et al.  Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN , 2005, Nature.

[14]  Newell Fw,et al.  [Typical monochromacy, congenital deafness, and resistance to intracellular action of thyroid hormone (author's transl)]. , 1977 .

[15]  M. Menaker,et al.  Light-Induced Phase Shifts in tau Mutant Hamsters , 1994, Journal of biological rhythms.

[16]  R. Refinetti.  Effects of Prolonged Exposure to Darkness on Circadian Photic Responsiveness in the Mouse , 2003, Chronobiology international.

[17]  S. Bloomfield,et al.  Rod Vision: Pathways and Processing in the Mammalian Retina , 2001, Progress in Retinal and Eye Research.

[18]  N. Mrosovsky.  FURTHER CHARACTERIZATION OF THE PHENOTYPE OF mCry1/mCry2-DEFICIENT MICE , 2001, Chronobiology international.

[19]  M. Biel,et al.  Melanopsin and rod–cone photoreceptive systems account for all major accessory visual functions in mice , 2003, Nature.

[20]  James W. Jenness.  Human Color Vision (Second Edition) , 1997 .

[21]  M. Kelley,et al.  Ligands of steroid/thyroid receptors induce cone photoreceptors in vertebrate retina. , 1995, Development.

[22]  K. Tsuji,et al.  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 , 1980, Physiology & Behavior.

[23]  N. Mrosovsky,et al.  Diurnal mice (Mus musculus) and other examples of temporal niche switching , 2005, Journal of Comparative Physiology A.

[24]  R. Foster,et al.  Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. , 1999, Science.

[25]  R. V. Van Gelder,et al.  Reduced Pupillary Light Responses in Mice Lacking Cryptochromes , 2003, Science.

[26]  D. Arendt,et al.  Ciliary Photoreceptors with a Vertebrate-Type Opsin in an Invertebrate Brain , 2004, Science.

[27]  J. Samarut,et al.  Different functions for the thyroid hormone receptors TRα and TRβ in the control of thyroid hormone production and post‐natal development , 1999 .

[28]  N. Mrosovsky.  Contribution of classic photoreceptors to entrainment , 2002, Journal of Comparative Physiology A.

[29]  D. Berson,et al.  Phototransduction by Retinal Ganglion Cells That Set the Circadian Clock , 2002, Science.

[30]  G. H. Jacobs,et al.  Retinal receptors in rodents maximally sensitive to ultraviolet light , 1991, Nature.

[31]  Samer Hattar,et al.  Central projections of melanopsin‐expressing retinal ganglion cells in the mouse , 2006, The Journal of comparative neurology.

[32]  Donald J. Zack,et al.  A locus control region adjacent to the human red and green visual pigment genes , 1992, Neuron.

[33]  M. Pinazo-Durán,et al.  Low Thyroid Hormone Levels Impair the Perinatal Development of the Rat Retina , 2002, Ophthalmic Research.

[34]  R. M. Boynton.  Human color vision , 1979 .

[35]  J. Samarut,et al.  Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development. , 1999, The EMBO journal.

[36]  S. Peirson,et al.  Melanopsin retinal ganglion cells and the maintenance of circadian and pupillary responses to light in aged rodless/coneless (rd/rd cl) mice , 2003, The European journal of neuroscience.

[37]  E. Nevo,et al.  Photopigments and circadian systems of vertebrates. , 1995, Biophysical chemistry.

[38]  Bruce F O'Hara,et al.  Role of Melanopsin in Circadian Responses to Light , 2002, Science.

[39]  J. Hurley,et al.  Scotopic and Photopic Visual Thresholds and Spatial and Temporal Discrimination Evaluated by Behavior of Mice in a Water Maze † , 2006 .

[40]  S. Kato,et al.  Distinct functions of photoreceptor cell-specific nuclear receptor, thyroid hormone receptor beta2 and CRX in one photoreceptor development. , 2002, Investigative ophthalmology & visual science.

[41]  R. Foster,et al.  Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. , 1999, Science.

[42]  Robert J. Lucas,et al.  Characterization of an ocular photopigment capable of driving pupillary constriction in mice , 2001, Nature Neuroscience.

[43]  G. E. Pickard,et al.  Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses , 2003, The Journal of comparative neurology.

[44]  G. Tosini,et al.  Classical Photoreceptors Regulate Melanopsin mRNA Levels in the Rat Retina , 2004, The Journal of Neuroscience.

[45]  Kwoon Y. Wong,et al.  Photoreceptor Adaptation in Intrinsically Photosensitive Retinal Ganglion Cells , 2005, Neuron.

[46]  T. Holy,et al.  Physiologic Diversity and Development of Intrinsically Photosensitive Retinal Ganglion Cells , 2005, Neuron.

[47]  C. Hawryshyn,et al.  Thyroxine induces a precocial loss of ultraviolet photo sensitivity in rainbow trout (Oncorhynchus mykiss, teleostei) , 1992, Vision Research.

[48]  Serge Daan,et al.  A functional analysis of circadian pacemakers in nocturnal rodents , 1976, Journal of comparative physiology.

[49]  O. Dkhissi-Benyahya,et al.  Effects of Irradiance and Stimulus Duration on Early Gene Expression (Fos) in the Suprachiasmatic Nucleus: Temporal Summation and Reciprocity , 2000, The Journal of Neuroscience.

[50]  D. Forrest,et al.  Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor beta: evidence for tissue‐specific modulation of receptor function. , 1996, The EMBO journal.

[51]  Satchidananda Panda,et al.  Melanopsin (Opn4) Requirement for Normal Light-Induced Circadian Phase Shifting , 2002, Science.

[52]  J. Hurley,et al.  Scotopic and Photopic Visual Thresholds and Spatial and Temporal Discrimination Evaluated by Behavior of Mice in a Water Maze† , 2006, Photochemistry and photobiology.

[53]  R. Foster,et al.  Circadian rhythms in mice can be regulated by photoreceptors with cone-like characteristics , 1995, Brain Research.

[54]  John D. Bullough,et al.  Additivity in Murine Circadian Phototransduction , 2005, Zoological science.