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Department of Psychological and Brain Sciences (G.F.B.), Johns Hopkins University, Baltimore, Maryland 21230 and University of Liège (J.B.), Center for Cellular and Molecular Neurobiology, B-4020 Liege, Belgium
Address all correspondence and requests for reprints to: Gregory F. Ball, Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 North Charles Street, Baltimore, Maryland 21230. E-mail: gball{at}jhu.edu.
One of the best known facts about natural history is surely that birds in the temperate zone tend to breed in the spring (1). Even a hardened urbanite notices the many changes associated with bird life that occur at this time, such as flocks of migrants passing overhead and marked increases in birdsong early in the morning. Despite the fact that these overt changes in activity are relatively well known, the underlying physiological systems that coordinate these changes remain unappreciated by many. Maintaining reproductive systems at full capacity is costly, especially to birds with their volant lifestyles. Therefore, these systems atrophy in seasonal breeders, often to a profound degree. To breed in the spring, birds must predict the vernal amelioration of the environment months in advance and gear up the reproductive neuroendocrine system so that they will be ready to fly to the right place, find and court a proper mate, obtain and perhaps construct a suitable nest site, lay eggs, and then incubate the eggs and care for the young. The paper by Yasuo et al. (2) in the current issue of Endocrinology provides us with new insights into the clock that is used to coordinate these complex hormonal changes. To understand completely the significance of these findings, we need to first review briefly what we do know about the neuroendocrine control of seasonal reproduction with a special emphasis on birds.
How do birds (and other seasonally breeding species) carry out this remarkable feat of seasonal breeding? A series of stunning discoveries going back to the 1920s have taught us much about this process. It was Rowan (3) who first observed during studies of migratory behavior in dark-eyed juncos (Junco hyemalis) that presenting birds with long day lengths could induce out-of-season migratory behavior. It subsequently became clear that seasonal variation in photoperiod is a key predictive cue used by birds to time both recrudescence and regression of the reproductive system at the appropriate times depending on the specifics of the natural history of the species in question (4, 5). Changes in photoperiod along with a host of supplementary cues that fine-tune reproductive recrudescence and regression, including factors such as variation in temperature and social interactions, provide the cues used by birds to time events properly for the maximization of reproductive success, even in the face of yearly variation in the progression of seasonal changes in the environment (6, 7). As the study of physiological mechanisms mediating seasonal reproduction and photoperiodism progressed, surprises were in store. Benoit (8) first observed in his study of photoperiodism in mallard ducks (Anas platyrhyncos) that the response to photoperiod involved sensory receptors in the brain itself rather than in the retina. It is now clear that an extraretinal photoreceptor present in the brain serves as the sensory detector for photoperiod in birds (9). Thus, a blind bird’s reproductive system responds appropriately to photoperiod, whereas blocking light shining through the skull consigns the bird to constant darkness (10). Given that birds clearly detect and use changes in photoperiod, how do they measure it? One appealing idea is that a physiological hourglass of some sort is involved. Some investigators tried to find evidence for the accumulation of a substance that would track either night length or day length (e.g. Ref.11). However, W. M. Hamner (12), borrowing from concepts applied to plants and insects by Bünning (13) and K.C. Hamner (14), demonstrated in house finches (Carpodacus mexicanus) that photoperiod is measured by the circadian system. One needs only two light pulses to stimulate a photoperiodic response, a dawn pulse and then a second pulse coincident with a particular phase of the circadian cycle (the photoinducible phase or 
i). A series of studies on both birds and mammals has demonstrated definitively that the photoperiodic time measurement system uses the circadian system to attain its goal (15, 16).
Where then is the circadian clock that does this job? In the 1970s, a consensus developed in the field of vertebrate rhythms that one key site for the activity of the circadian clock is the suprachiasmatic nucleus (SCN) (17). Simultaneous studies of photoperiodic mammals revealed that the pineal hormone melatonin codes for night length (plasma concentrations are high when it is dark and low when it is light). This code is used by seasonally breeding mammalian species such as hamsters and sheep to provide the circadian read-out needed for photoperiodic time measurement (18). A neural circuit was then identified starting with the retina projecting directly to the SCN that in turn projects to the paraventricular nucleus that then projects outside the brain to the superior cervical ganglion that ultimately projects to the pineal gland (19). Any interruption of this circuit blocked the rhythmic secretion of melatonin and, therefore, photoperiodic time measurement (19). However, in birds, this story did not seem to apply. Avian species do exhibit robust melatonin rhythms like mammals, but, curiously, they do not seem to use them for photoperiodic time measurement (20). Decades of experiments manipulating either the pineal or melatonin in a variety of avian species found no effect on the photoperiodic regulation of reproductive physiology (20). The putative site of the SCN in birds was also not obvious. Two candidate nuclei emerged, (21) and lesions to this general area did not provide clear proof for the interruption of photoperiodic time measurement (22).
The recent explosion in our knowledge about the molecular basis of circadian clocks has provided chronobiologists with a new opportunity to study the location of cells that can function as oscillators and therefore act as biological clocks. Yasuo et al. (2) conducted investigations of the rhythmic activity of the five clock genes that have been subcloned in birds (Fig. 1
). They studied clock gene expression in the brain and pineal gland of Japanese quail (Coturnix japonica) using in situ hybridization histochemistry methods. The quail were maintained on either long [16 h light, 8 h dark (16L:8D)] or short [8 h light, 16 h dark (8L:16D)] days or were placed in a night interruption experiment. In the night interruption groups, the birds were maintained on very short days [4 h light, 20 h dark (4L:20D)] and were given 30-min light pulses at different intervals of time from the onset of dawn (7, 14, or 21 h). The birds experiencing the pulse at 14 h exhibit gonadal growth because the light pulse is coincident with the photoinducible phase of their circadian cycle. Clock gene rhythmicity was observed in the SCN and the pineal, although the pattern of gene expression did change with photoperiod. However, in the medial basal hypothalamus, especially in nuclei dorsolateral to the median eminence, strong rhythmicity was also observed that was constant in all photoperiodic conditions (Fig. 1). This observation alone might not be significant, but several lines of evidence had previously suggested that this brain area is important for photoperiodic time measurement. For example, lesions to this area were found to block photostimulation in quail even when it was clear that there was no interference with the adjacent fibers immunoreactive for GnRH that is essential for pituitary function (23). The immediate early gene fos is expressed in this region specifically in association with photostimulation (24). Taken together, these data suggest that this brain area is the long-sought clock essential for photoperiodic time measurement in birds. Also, there is evidence that this area is a site of the encephalic photoreceptor itself (25). Therefore, many of the major components of the system required for the control of avian photoperiodism are present in the medial basal hypothalamus. Lesion studies indicating that this area is important in controlling at least some traits regulated by photoperiod in hamsters such as gonadal growth (26) suggest that it will be worth assessing carefully whether this region plays a general role among vertebrate species in the control of photoperiodic time measurement.
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Abbreviation: SCN, Suprachiasmatic nucleus.
Received June 24, 2003.
Accepted for publication July 2, 2003.
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This article has been cited by other articles:
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  N. Nakao, H. Ono, and T. Yoshimura Thyroid hormones and seasonal reproductive neuroendocrine interactions Reproduction, July 1, 2008; 136(1): 1 - 8. [Abstract] [Full Text] [PDF]
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