Photoentrainment in blind and sighted rodent species: Responses to photophase light with different wavelengths

Journal of Experimental Biology

Volumn 213, Issue 24, 2010, Pages 4213-4222

  Zubidat, Abed E ^a   Nelson, Randy J ^b   Haim, Abraham ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Cosinor analysis; Masking; Melanopsin; Retinal photoreceptor; Subterranean

Indexed keywords

6 HYDROXYMELATONIN O SULFATE; 6-SULFATOXYMELATONIN; ADRENALIN; DRUG DERIVATIVE; HYDROCORTISONE; MELATONIN;

ANIMAL; ARTICLE; ARVICOLINAE; CHEMISTRY; CIRCADIAN RHYTHM; COMPARATIVE STUDY; MALE; METABOLISM; MICTURITION; MOLE RAT; OXYGEN CONSUMPTION; PHYSIOLOGY; RADIATION EXPOSURE; SPECIES DIFFERENCE; SUNLIGHT; URINE; VISION;

ANIMALS; ARVICOLINAE; CIRCADIAN RHYTHM; EPINEPHRINE; HYDROCORTISONE; MALE; MELATONIN; OXYGEN CONSUMPTION; SPALAX; SPECIES SPECIFICITY; SUNLIGHT; URINATION; URINE; VISION, OCULAR;

MAMMALIA; MICROTUS SOCIALIS; NANNOSPALAX EHRENBERGI; RODENTIA; SPALACINAE;

EID: 78650070705     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.048629     Document Type: Article

References (72)

1. Aral, E., Uslu, S., Sunal, E., Sariboyaci, A. E., Okar, I. and Aral, E. (2006). Response of the pineal gland in rats exposed to three different light spectra of short periods. Turk. J. Anim. Sci. 30, 29-34.
2. Arendt, J. (1985). Mammalian pineal rhythms. Pineal Res. Rev. 3, 161-213.
3. Avivi, A., Oster, H., Joel, A., Beiles, A., Albrecht, U. and Nevo, E. (2004). Circadian genes in a blind subterranean mammal III: Molecular cloning and circadian regulation of cryptochrome genes in the blind subterranean mole rat, Spalax ehrenbergi superspecies. J. Biol. Rhythms 19, 22-34.
4. Banin, D., Haim, A. and Arad, Z. (1994). Metabolism and thermoregulation in the Levant vole Microtus guentheri: The role of photoperiodicity. J. Therm. Biol. 19, 55-62.
5. Ben-Shlomo, R., Nevo, E., Ritte, U., Steinlechner, S. and Klante, G. (1996). 6- Sulphatoxymelatonin secretion in different locomotor activity types of the blind mole rat Spalax ehrenbergi. J. Pineal Res. 21, 243-250.
6. Benjamini, L. (1989). Diel activity rhythms in the Levent vole, Microtus guentheri. Isr. J. Zool. 47, 194-195.
7. Bennett, A. F. and Ruben, J. A. (1979). Endothermy and activity in vertebrates. Science 206, 649-654.
8. Berson, D. M. (2007). Phototransduction in ganglion-cell photoreceptors. Pflugers Arch. 454, 849-855.
9. Bingham, C., Arbogast, B., Guillaume, G. C., Lee, J. K. and Halberg, F. (1982). Inferential statistical methods for estimating and comparing cosinor parameters. Chronobiologia 9, 397-439.
10. Broughton, R. J. (1985). Three central issues concerning ultradian rhythms. In Ultradian Rhythms in Physiology and Behavior (ed. H. Schulz and P. Lavie), pp. 217-233. New York: Springer-Verlag.
11. Bullough, J. D., Rea, M. S. and Figueiro, M. G. (2006). Of mice and women: Light as a circadian stimulus in breast cancer research. Cancer Causes Control 17, 375-383.
12. Cernuda-Cernuda, R., DeGrip, W. J., Cooper, H. M., Nevo, E. and García-Fernández, J. M. (2002). The retina of Spalax ehrenbergi: Novel histologic features supportive of a modified photosensory role. Invest. Ophthalmol. Vis. Sci. 43, 2374-2383.
13. Chávez, A. E., Bozinovic, F., Peichl, L. and Palacios, A. G. (2003). Retinal spectral sensitivity, fur coloration, and urine reflectance in the genus octodon (rodentia): Implications for visual ecology. Invest. Ophthalmol. Vis. Sci. 44, 2290-2296.
14. Cooper, H. M., Herbin, M. and Nevo, E. (1993). Visual system of a naturally microphthalmic mammal: The blind mole rat, Spalax ehrenbergi. J. Comp. Neurol. 328, 313-350.
15. Daan, S. and Aschoff, J. (1982). Circadian contributions to survival. In Vertebrate Circadian Rhythms (ed. J. Aschoff, S. Daan and G. A. Groos), pp. 305-321. New York: Springer.
16. David-Gray, Z. K., Janssen, J. W., DeGrip, W. J., Nevo, E. and Foster, R. G.(1998). Light detection in a 'blind' mammal. Nat. Neurosci. 1, 655-656.
17. Dickmeis, T. (2009). Glucocorticoids and the circadian clock. J. Endocrinol. 200, 3-22.
18. Droste, S. K., de Groote, L., Atkinson, H. C., Lightman, S. L., Reul, J. M. and Linthorst, A. C. (2008). Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology 149, 3244-3253.
19. Dunn, A. J. and Swiergiel, A. H. (2008). The role of corticotropin- releasing factor and noradrenaline in stress-related responses, and the inter-relationships between the two systems. Eur. J. Pharmacol. 583, 186-193.
20. Gerkema, M. P., Groos, G. A. and Daan, S. (1990). Differential elimination of circadian and ultradian rhythmicity by hypothalamic lesions in the common vole, Microtus arvalis. J. Biol. Rhythms 5, 81-95.
21. Goldman, B. D., Goldman, S. L., Riccio, A. P. and Terkel, J. (1997). Circadian patterns of locomotor activity and body temperature in blind mole-rats, Spalax ehrenbergi. J. Biol. Rhythms 12, 348-361.
22. Goldstein, D. S. and Kopin, I. J. (2008). Adrenomedullary, adrenocortical, and sympathoneural responses to stressors: A meta-analysis. Endocr. Regul. 42, 111-119.
23. Gouthiere, L., Mauvieux, B., Davenne, D. and Waterhouse, J. (2005). Complementary methodology in the analysis of rhythmic data, using examples from a complex situation, the rhythmicity of temperature in night shift workers. Biol. Rhythm Res. 36, 177-193.
24. Graham, D. M., Wong, K. Y., Shapiro, P., Frederick, C., Pattabiraman, K. and Berson, D. M. (2008). Melanopsin ganglion cells use a membrane-associated rhabdomeric phototransduction cascade. J. Neurophysiol. 99, 2522-2532.
25. Güler, A. D., Altimus, C. M., Ecker, J. L. and Hattar, S. (2007). Multiple photoreceptors contribute to nonimage-forming visual functions predominantly through melanopsin-containing retinal ganglion cells. Cold Spring Harbor Symp. Quant. Biol. 72, 509-515.
26. Güler, A. D., Ecker, J. L., Lall, G. S., Haq, S., Altimus, C. M., Liao, H. W., Barnard, A. R., Cahill, H., Badea, T. C., Zhao, H. et al. (2008). Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453, 102-105.
27. Haim, A., Heth, G., Pratt, H. and Nevo, E. (1983). Photoperiodic effects on thermoregulation in a 'blind' subterranean mammal. J. Exp. Biol. 107, 59-64.
28. Haim, A., Zubidat, A. E. and Scantelbury, M. (2005). Seasonal and seasons out of time-thermoregulatory effects of light interference. Chronobiol. Int. 22, 57-64.
29. Hankins, M. W., Peirson, S. N. and Foster, R. G. (2008). Melanopsin: An exciting photopigment. Trends Neurosci. 31, 27-36.
30. Hannibal, J., Hindersson, P., Nevo, E. and Fahrenkrug, J. (2002). The circadian photopigment melanopsin is expressed in the blind subterranean mole rat, Spalax. Neuroreport 13, 1411-1414.
31. Harrison, D. L. and Bates, P. J. (1991). The Mammals of Arabia, 2nd edn, pp. 309- 313. Kent: Harrison Zoological Museum Publication.
32. Janssen, J. W., Bovee-Geurts, P. H., Peeters, Z. P., Bowmaker, J. K., Cooper, H. M., David-Gray, Z. K., Nevo, E. and DeGrip, W. J. (2000). A fully functional rod visual pigment in a blind mammal. A case for adaptive functional reorganization?. J. Biol. Chem. 275, 38674-38679.
33. Janssen, J. W., David-Gray, Z. K., Bovee-Geurts, P. H., Nevo, E., Foster, R. G. and DeGrip, W. J. (2003). A green cone-like pigment in the 'blind' mole-rat Spalax ehrenbergi: Functional expression and photochemical characterization. Photochem. Photobiol. Sci. 2, 1287-1291.
34. Kalsbeek, A., Perreau-Lenz, S. and Buijs, R. M. (2006). A network of (autonomic) clock outputs. Chronobiol. Int. 23, 201-215. (Pubitemid 43739032)
35. Kavakli, I. H. and Sancar, A. (2002). Circadian photoreception in humans and mice. Mol. Interv. 2, 484-492.
36. Klerman, E. B., Shanahan, T. L., Brotman, D. J., Rimmer, D. W., Emens, J. S., Rizzo, J. F. and Czeisler, C. A. (2002). Photic resetting of the human circadian pacemaker in the absence of conscious vision. J. Biol. Rhythms 17, 548-555.
37. Kumar, V. and Rani, S. (1999). Light sensitivity of the photoperiodic response system in higher vertebrates: Wavelength and intensity effects. Indian J. Exp. Biol. 37, 1053-1064.
38. Lightman, S. L. (2008). The neuroendocrinology of stress: A never ending story. J. Neuroendocrinol. 20, 880-884.
39. Lloyd, D. and Stupfel, M. (1991). The occurrence and functions of ultradian rhythms. Biol. Rev. Camb. Philos. Soc. 66, 275-299.
40. Lucas, R. J., Freedman, M. S., Munoz, M., Garcia-Fernandez, J. M. and Foster, R. G. (1999). Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science 284, 505-507. (Pubitemid 29289627)
41. Mrosovsky, N. and Hattar, S. (2003). Impaired masking responses to light in melanopsin-knockout mice. Chronobiol. Int. 20, 989-999.
42. Mrosovsky, N., Foster, R. G. and Salmon, P. A. (1999). Thresholds for masking responses to light in three strains of retinally degenerate mice. J. Comp. Physiol. A 184, 423-428.
43. Mrosovsky, N., Salmon, P. A., Foster, R. G. and McCall, M. A. (2000). Responses to light after retinal degenerationn. Vision Res. 40, 575-578.
44. Mure, L. S., Rieux, C., Hattar, S. and Cooper, H. M. (2007). Melanopsin-dependent nonvisual responses: Evidence for photopigment bistability in vivo. J. Biol. Rhythms 22, 411-424.
45. Nakahara, D., Nakamura, M., Iigo, M. and Okamura, H. (2003). Bimodal circadian secretion of melatonin from the pineal gland in a living CBA mouse. Proc. Natl. Acad. Sci. USA 100, 9584-9589.
46. Navara, K. J. and Nelson, R. J. (2007). The dark side of light at night: Physiological, epidemiological, and ecological consequences. J. Pineal Res. 43, 215-224.
47. Nelson, W., Tong, Y., Lee, J. and Halberg, F. (1979). Methods for cosinorrhythmometry. Chronobiologia 6, 305-323.
48. Nevo, E. (1999). Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence. Oxford: Oxford University Press.
49. Nevo, E., Ivanitskaya, E. and Beiles, A. (2001). Adaptive Radiation of Blind Subterranean Mole Rats. Leiden, Netherlands: Backhuys.
50. Panda, S., Nayak, S. K., Campo, B., Walker, J. R., Hogenesch, J. B. and Jegla, T. (2005). Illumination of the melanopsin signaling pathway. Science 307, 600-604.
51. Pandi-Perumal, S. R., Trakht, I., Srinivasan, V., Spence, D. W., Maestroni, G. J., Zisapel, N. and Cardinali, D. P. (2008). Physiological effects of melatonin: Role of melatonin receptors and signal transduction pathways. Prog. Neurobiol. 85, 335-353.
52. Peichl, L. (2005). Diversity of mammalian photoreceptor properties: Adaptations to habitat and lifestyle? Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 287, 1001-1012.
53. Pévet, P., Agez, L., Bothorel, B., Saboureau, M., Gauer, F., Laurent, V. and Masson-Pévet, M. (2006). Melatonin in the multi-oscillatory mammalian circadian world. Chronobiol. Int. 23, 39-51.
54. Rado, R., Gev, H., Goldamn, B. D. and Terkel, J. (1991). Light and circadian activity in the blind mole rat. In Photobiology (ed. E. Riklis), pp. 581-589. New York: Plenum.
55. Refinetti, R., Cornélissen, G. and Halberg, F. (2007). Procedures for numerical analysis of circadian rhythms. Biol. Rhythm Res. 38, 275-325.
56. Reiter, R. J. (1994). Non-visible electromagnetic radiation and pineal function. Eye- Pineal Relationships International Symposium, Nencki Institute Warszawa. Acta Neurobiol. Exp. 54, 93-94.
57. Sanyal, S., Jansen, H. G., de Grip, W. J., Nevo, E. and de Jong, W. W. (1990). The eye of the blind mole rat, Spalax ehrenbergi. Rudiment with hidden function? Invest. Ophthalmol. Vis. Sci. 31, 1398-1404.
58. Speakman, J. (2000). The cost of living: Field metabolic rates of small mammals. Adv. Ecol. Res. 30, 177-297.
59. Taylor, C. R. and Heglund, N. C. (1982). Energetics and mechanics of terrestrial locomotion. Annu. Rev. Physiol. 44, 97-107.
60. Taylor, C. R., Heglund, N. C. and Maloiy, G. M. (1982). Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals. J. Exp. Biol. 97, 1-21.
61. Tendron-Franzin, A., Gouyon, J. B., Guignard, J. P., Decramer, S., Justrabo, E., Gilbert, T. and Semama, D. S. (2004). Long-term effects of in utero exposure to cyclosporin A on renal function in the rabbit. J. Am. Soc. Nephrol. 15, 2687-2693.
62. Thompson, S., Foster, R. G., Stone, E. M., Sheffield, V. C. and Mrosovsky, N. (2008). Classical and melanopsin photoreception in irradiance detection: Negative masking of locomotor activity by light. Eur. J. Neurosci. 27, 1973-1979.
63. Ulrich-Lai, Y. M. and Herman, J. P. (2009). Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10, 397-409.
64. Van Gelder, R. N. (2005). Nonvisual ocular photoreception in the mammal. Methods Enzymol. 393, 746-755.
65. Wehr, T. A., Schwartz, P. J., Turner, E. H., Feldman-Naim, S., Drake, C. L. and Rosenthal, N. E. (1995). Bimodal patterns of human melatonin secretion consistent with a two-oscillator model of regulation. Neurosci. Lett. 194, 105-108.
66. Zawilska, J. B., Skene, D. J. and Arendt, J. (2009). Physiology and pharmacology of melatonin in relation to biological rhythms. Pharmacol. Rep. 61, 383-410.
67. Zubidat, A. E. and Haim, A. (2007). The effect of alpha- and beta-adrenergic blockade on daily rhythms of body temperature, urine production, and urinary 6- sulfatoxymelatonin of social voles Microtus socialis. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 148, 301-307.
68. Zubidat, A. E., Ben-Shlomo, R. and Haim, A. (2007). Thermoregulatory and endocrine responses to light pulses in short-day acclimated M. socialis (Microtus socialis). Chronobiol. Int. 24, 269-288.
69. Zubidat, A. E., Nelson, R. J. and Haim, A. (2008). Urinary adrenalin and cortisol secretion patterns of M. socialis in response to adrenergic blockade under basal conditions. Physiol. Behav. 93, 243-249.
70. Zubidat, A. E., Nelson, R. J. and Haim, A. (2009). Photosensitivity to different light intensities in blind and sighted rodents. J. Exp. Biol. 212, 3857-3864.
71. Zubidat, A. E., Nelson, R. J. and Haim, A. (2010). Differential effects of photophase irradiance on metabolic and urinary stress hormone concentrations in 'blind' and sighted rodents. Chronobiol. Int. 27, 487-516.
72. Zuri, I. and Terkel, J. (1996). Locomotor patterns, territory, and tunnel utilization in the mole-rat Spalax ehrenbergi. J. Zool. 240, 123-140.