Extraretinal Light Perception in the Sparrow, III: The Eyes Do Not Participate in Photoperiodic Photoreception

Abstract

Abstract. Photoperiodic control of testis growth in Passer domesticus (house sparrow) is mediated entirely by extraretinal photoreceptors in the brain. The eyes do not participate in photoperiodically significant photoreception. Removal of the pineal organ does not affect either the response to light or, to a first approximation, the process of recrudescence. The intensity of light reaching the retina and that reaching the extraretinal photoreceptor were varied independently. This technique will make it possible to study brain photoreception in species of birds that will not tolerate blinding. Extreme caution is necessary in the interpretation of brain lesion experiments in which reproductive function is modified, since photoreception by brain receptors of unknown anatomical location affects testicular state.In an earlier paper in this series1 we reported that seemingly normal testis growth occurred in Passer domesticus exposed to inductive daylengths even though the eyes had been surgically removed. We concluded that an extraretinal photoreceptor (ERR,-extraretinal receptor for photoperiodism) must be involved in the control of testicular recrudescence and speculated on the role of retinal light perception in the intact bird. Benoit has argued that both a retinal and a brain photoreceptor are involved in the testis response of ducks.2 We discussed his arguments and concluded that the question of whether the eyes were involved at all, remained open. We have since demonstrated3 that there are no significant differences in either rate or extent of testis growth in blinded, as opposed to unoperated, sparrows held on the same lighting regimen. This result was confirmed at several different photoperiods, light intensities, and times of year; and strongly suggests, although it does not prove, that retinal light perception is not involved in photoperiodically-mediated reproductive control in P. domesticus.We have shown that the synchronization (entrainment) of the circadian rhythm of activity in the sparrow is also mediated by an extraretinal light receptor (ERR,-extraretinal receptor for entrainment).4 Further, this receptor must be in the brain, as the behavioral response to light cycles can be manipulated by affecting the amount of light that penetrates the head.5The present paper applies techniques that have been shown to affect the amount of light reaching the ERR. to the study of photoperiodically-controlled 320

Light-harvesting chlorophyll pigments enable mammalian mitochondria to capture photonic energy and produce ATP

“…In humans, the temporal bone of the skull and the scalp attenuate only 50% of light at a wavelength of ,670 nm (Eichler et al, 1977;Wan et al, 1981). In small animals, light can readily reach the entire brain under normal illumination (Berry and Harman, 1956;Massopust and Daigle, 1961;Menaker et al, 1970;Vanbrunt et al, 1964). Sun or room light over the range of 600-700 nm can penetrate an approximately 4-cm-thick abdominal wall with only three-to-five orders of magnitude attenuation (Bearden et al, 2001;Wan et al, 1981).…”

“…Given estimated concentrations of chlorophyll derivatives in the body (Egner et al, 2000;Fernandes et al, 2007;Scheie and Flaoyen, 2003) and the photon flux at 670 nm (Bachem and Reed, 1931;Barun et al, 2007;Bearden et al, 2001;Benaron et al, 1997;Chance et al, 1988;Eichler et al, 1977;Menaker et al, 1970;Vanbrunt et al, 1964;Wan et al, 1981;Zourabian et al, 2000), each chlorophyll metabolite would be expected to absorb only a few photons per second. As such, one might anticipate negligible amounts of additional energy.…”

The saccus vasculosus of fish is a sensor of seasonal changes in day length

“…In birds, by contrast, melatonin has little effect on photoperiodic response of gonads 8 . Furthermore, neither eyes nor the pineal organ, another photoreceptive organ in non-mammalian vertebrates, are necessary for the photoperiodic response in birds 9 ; instead, light received by the deep-brain photoreceptors induces expression of TSH in the PT 10 . Most fish living outside the tropics also exhibit a photoperiodic response 11 , and involvement of thyroid hormone in the regulation of seasonal reproduction has been described extensively 12 .…”

Molecular basis for regulating seasonal reproduction in vertebrates

“…In addition to photoreceptors in the retina, nonmammalian vertebrates have extraretinal photoreceptors located in the pineal gland (Okano et al 1994) and the brain; deep brain photoreceptors are thought to be responsible for avian photoperiodism (Benoit 1935, Menaker et al 1970. As expected, photoperiodicity is not disrupted by the removal of the eyes or pineal gland in quail (Siopes & Wilson 1974).…”