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The Journal of Neuroscience, December 1, 2002, 22(23):10427-10433

Loss of Photic Entrainment and Altered Free-Running Circadian Rhythms in math5^/ Mice

Raymond Wee¹, Ana Maria Castrucci³, Ignacio Provencio³, Lin Gan⁴, and Russell N. Van Gelder^{1, 2}

Departments of ¹ Ophthalmology and Visual Sciences and ² Molecular Biology and Pharmacology, Washington University Medical School, St. Louis, Missouri 63110, ³ Department of Anatomy, Physiology, and Genetics, Uniformed Services University of Health Sciences, Bethesda, Maryland 20814, and ⁴ Department of Neurobiology and Anatomy, University of Rochester Medical School, Rochester, New York 14642

Mammalian free-running circadian rhythms are entrained to the external light/dark cycle by photic signaling to the suprachiasmatic nuclei via the retinohypothalamic tract (RHT). We investigated the circadian entrainment and clock properties of math5^/ mutant mice. math5 is a critical regulator of retinal ganglion cell development; math5^/ mice show severe optic nerve hypoplasia. By anterograde cholera toxin B tracing, we find that math5^/ mice do not develop an identifiable RHT pathway. This appears to be attributable to agenesis or dysgenesis of the majority of RHT-projecting retinal ganglion cells. math5^/ mice display free-running circadian rhythms with a period ~1 hr longer than B6/129 controls (24.43 ± 0.10 vs 23.62 ± 0.19 hr; p < 0.00001). The free-running period of heterozygote mice is indistinguishable from that of controls. math5^/ mice show no entrainment to light/dark cycles, whereas heterozygote mice show normal entrainment to both 12 hr light/dark cycles and to a 1 hr skeletal photoperiod. math5^/ mice show reduced ability to entrain their rhythms to the nonphotic time cue of restricted running wheel access but demonstrate both free-running behavior and entrained anticipation of wheel unlocking in these conditions, suggesting the presence of a second diurnal oscillatory system in math5^/ animals. These results demonstrate that retinal ganglion cell input is not necessary for the development of a free-running circadian timekeeping system in the suprachiasmatic nucleus but is important for both photic entrainment and determination of the free-running period.

Key words: circadian rhythm; math5; photic entrainment; retinohypothalamic tract; nonphotic entrainment; phase shifting

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Copyright © 2002 Society for Neuroscience  0270-6474/02/222310427-07$05.00/0

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