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Endocrinology, doi:10.1210/en.2003-0435
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Endocrinology Vol. 144, No. 9 3742-3748
Copyright © 2003 by The Endocrine Society

Circadian Clock Genes and Photoperiodism: Comprehensive Analysis of Clock Gene Expression in the Mediobasal Hypothalamus, the Suprachiasmatic Nucleus, and the Pineal Gland of Japanese Quail under Various Light Schedules

Shinobu Yasuo, Miwa Watanabe, Naritoshi Okabayashi, Shizufumi Ebihara and Takashi Yoshimura

Division of Biomodeling, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan

Address all correspondence and requests for reprints to: Takashi Yoshimura, Ph.D., Division of Biomodeling, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan. E-mail: takashiy{at}agr.nagoya-u.ac.jp.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
In birds, the mediobasal hypothalamus (MBH) including the infundibular nucleus, inferior hypothalamic nucleus, and median eminence is considered to be an important center that controls the photoperiodic time measurement. Here we show expression patterns of circadian clock genes in the MBH, putative suprachiasmatic nucleus (SCN), and pineal gland, which constitute the circadian pacemaker under various light schedules. Although expression patterns of clock genes were different between long and short photoperiod in the SCN and pineal gland, the results were not consistent with those under night interruption schedule, which causes testicular growth. These results indicate that different expression patterns of the circadian clock genes in the SCN and pineal gland are not an absolute requirement for encoding and decoding of seasonal information. In contrast, expression patterns of clock genes in the MBH were stable under various light conditions, which enables animals to keep a steady-state photoinducible phase.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
REPRODUCTION OF MANY temperate-zone birds is under photoperiodic control. Although melatonin has an important role for the regulation of the photoperiodic time measurement (PTM) in mammals, no effect of melatonin manipulations is observed in birds (1). Japanese quail is an appropriate model system for the investigation of the PTM because of its rapid and dramatic response to photoperiod. Therefore, a considerable number of studies have been made on Japanese quail over the past few decades. Numerous reports have suggested that the mediobasal hypothalamus (MBH), including the infundibular nucleus (IN), inferior hypothalamic nucleus (IH), and median eminence (ME), is an important center controlling the PTM. For example, lesions of the IN, ME, or nucleus hypothalamicus posterior medialis, also known as nucleus medialis hypothalami posterioris or nucleus ventromedialis hypothalami, within the MBH can block the rise of LH and testicular growth under long photoperiods (2, 3, 4). In the lesion study, block of the photoperiodic response is effective, even though the GnRH system has been left intact (5). In addition, electrical stimulation of the IN and IH increases LH secretion (6) and induces testicular growth (7). Furthermore, Meddle and Follett (8, 9) have shown the expression of Fos-like immunoreactivity in the IN, IH, and ME by photostimulation of one long day.

It is an established fact that the circadian clock is involved in the PTM (10). Recently homologs of mammalian circadian clock genes including Clock, Per2, Per3, Bmal1, Cry1, Cry2, and E4bp4 have been cloned in birds, which provided a way to examine a molecular link between circadian clock and photoperiodism in birds (11, 12, 13, 14, 15, 16).

In the present study, we examined the expression of all known avian circadian clock genes (Clock, Per2, Per3, Bmal1, Cry1, Cry2, and E4bp4) under long days, short days, and night interruption schedules in the MBH, a center for the PTM and putative suprachiasmatic nucleus (SCN), the pineal gland that constitutes the circadian pacemakers (17), to understand the relationship between clock genes and the PTM.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Animals and housing
Four-week-old Japanese quail (Coturnix coturnix japonica) were obtained from a local dealer and housed in light tight-boxes in which light cycles were provided. The boxes were placed in a room at a temperature of 24 ± 1 C. Birds were maintained under 8:16 h light/dark cycle (LD) to examine the effect of long-day and short-day condition or LD 4:20 cycles to examine the effect of night interruption schedule until the experiment. Light was supplied by fluorescent lamps with a light intensity of 200 lux measured at the level of the bird’s head. Food and water were available ad libitum and were replenished at least once a week. Animals were treated in accordance with the guidelines of Nagoya University.

Expression patterns of clock genes under long day and short day
We examined the expression of clock genes under short days and long days. In the case of long days, birds were maintained under LD 16:8 for at least 2 wk before sampling, and under short days, they were raised under LD 8:16 from 4–9 wk of age. We examined expression patterns of clock genes in the MBH, SCN, and pineal gland.

Expression patterns of clock genes under night interruption schedules
Birds were raised under LD 4:20 from 4–9 wk old and divided into three groups randomly. Light pulses of 30 min were given during the dark periods for 10 consecutive days: group 1, zeitgeber time (ZT) 7 (LDLD 4:3:0.5:16.5); group 2, ZT14 (LDLD 4:10:0.5:9.5); group 3, ZT21 (LDLD 4:17:0.5:2.5). Birds were killed on the d 11 at several time points, and the weight of paired testes was measured. Because activity of animals given light pulses at ZT21 starts from ZT21 (18), we regarded the light pulse at ZT21 as the light onset of the day and compared the results.

In situ hybridization
Birds were killed by decapitation, and the brains were immediately removed to avoid acute changes in gene expression. Sampling was conducted at ZT 2, 6, 10, 14, 18, and 22 in all experiments. In situ hybridization was carried out according to a previous report (11). Antisense 45 mer oligonucleotide probes (qPer2: nucleotides 1904–1948 of GenBank accession no. AB029890; qPer3: 1382–1426 of AB029891; qClock: 861–905 of AB29889; cBmal1: 51–95 of AF205219; cCry1: 1742–1786 of AY034432; cCry2: 1657–1701 of AY034433; cE4bp4: 421–465 of AF335427) were labeled with [33P]dATP (NEN Life Science Products, Boston, MA) using terminal deoxyribonucleotidyl transferase (Gibco, Frederick, MD). Hybridization was carried out overnight at 42 C. Washing was carried out at room temperature for 30 min and at 55 C for 40 min twice. After washing, they were exposed to Biomax-MR film (Kodak, Rochester, NY) for 2 wk. 14C standards (American Radiolabeled Chemicals, St. Louis, MO) were included in each cassette, and densitometric analysis was carried out using a computed image-analyzing system (MCID, Imaging Research, St. Catherines, Ontario, Canada) to convert signal intensity into the relative OD (ROD). As a background, the ROD of the region of stratum cellulare internum [in cases of the MBH, pineal, and pars tuberalis (PT)] or the nucleus periventricularis magnocelluralis (in cases of the SCN) was measured and subtracted from all RODs.

Statistical analysis
Rhythmicity of each gene expression was analyzed with one-way factorial ANOVA using Fisher’s least significant difference (LSD) post hoc test (see Figs. 3Go, 5Go, and 7Go). Effect of day length on each gene’s expression profile was examined by two-way factorial ANOVA (see Figs. 3Go and 5AGo). When a significant difference was observed using two-way factorial ANOVA (shown by black asterisks), the difference at each time point was analyzed by t test (shown by blue asterisks) (see Figs. 3Go and 5AGo). Differences between paired testes weight were examined by one-way factorial ANOVA using Fisher’s LSD post hoc test. Values of each time point under three different light conditions were examined by one-way factorial ANOVA using Fisher’s LSD post hoc test (see Figs. 5BGo and 7Go, shown by blue asterisks).



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  		FIG. 3. Temporal expression profiles of clock genes in the MBH, SCN, and pineal gland under long days (LD 16:8, red open square) and short days (LD 8:16, green closed square). The bar at the bottom of each graph represents the light condition. Significant differences between long and short days revealed by two-way factorial ANOVA (black asterisks, P < 0.05). Difference at each time point is analyzed by t test (blue asterisks, P < 0.05; double blue asterisks, P < 0.01). Each value is the mean ± SEM (n = 3–6). Note that the scale for each graph is different.

 


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  		FIG. 5. Temporal expression patterns of Per2 and E4bp4 in the PT under long and short days (A) and night interruption light schedules (B). The bar at the bottom of each graph represents the light condition. Significant differences between long and short days revealed by two-way factorial ANOVA (black asterisks, P < 0.05). Difference at each time point is analyzed by t test (blue asterisks, P < 0.05). Each value is the mean ± SEM (n = 3–6). No significant differences were observed between photoinducible light cycles and nonphotoinducible light cycles (one-way factorial ANOVA). Note that the scale for each graph is different.

 


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  		FIG. 7. Temporal expression profiles of clock genes in the MBH, SCN, and pineal gland under night interruption light schedules. The light pulse of 30 min was given for 10 d at ZT7 (green up-pointing triangle), ZT14 (red open circle), or ZT21 (green down-pointing triangle) under LD 4:20 cycle. The bar at the bottom of each graph represents the light conditions. Because activity of animals given light pulses at ZT21 starts from ZT21 (18 ), we regard the light pulse at ZT21 as the light onset of the day. Significant differences in mRNA expression between photoinducible light cycle (ZT14) and nonphotoinducible light cycles (ZT7 and ZT21) are shown by asterisks (one-way factorial ANOVA: blue asterisks, P < 0.05; double blue asterisks, P < 0.01). Each value is the mean ± SEM (n = 3–6). Note that the scale for each graph is different.

 

   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Localization of clock gene expression in the MBH, SCN, and pineal gland
All clock genes examined in this study (Clock, Per2, Per3, Bmal1, Cry1, Cry2, and E4bp4) were expressed in the MBH including the IN, IH, and ME (Figs. 1Go and 2Go). In the central to caudal part of the MBH, the expression of the clock genes was observed in the entire part of the IH and IN, and no clear boundary between these nuclei was observed (Fig. 2Go, B and C). (Hereafter the region including the IH and IN is designated as the IN-IH.) All genes were also expressed in the PT, which is located just ventral to the ME (only the result of Per2 is shown in Fig. 2Go). We also confirmed that all genes were expressed in the SCN and pineal gland (Fig. 1Go). Although it is reported that the Per2 gene is expressed in the lateral hypothalamus as well as the SCN in house sparrow (19), we could not detect any signal in this comprehensive analysis, which is consistent with our previous studies (17, 20). Signals were also observed in the cerebellum and the optic tectum.



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  		FIG. 1. Representative autoradiographs of clock genes expression in the SCN, pineal gland, and MBH in Japanese quail. Samples at ZT6 for Per2, Cry1; ZT2 for Per3, Cry2; ZT10 or 14 for Clock, Bmal1, and E4bp4 were used. Signals were also observed in the cerebellum and optic tectum.

 


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  		FIG. 2. Detailed localization of Per2 expression in the MBH. Rostral (A), central (B), and caudal (C) regions of the MBH were shown, respectively. On the left top of each panel, an enlarged picture of the MBH and its schematic drawing are shown, respectively.

 
Temporal expression patterns of clock genes in the MBH, SCN, and pineal gland under long and short days
Temporal expression patterns of clock genes in the IN, IH, and ME were examined under long days (LD 16:8) and short days (LD 8:16). Because the expression patterns in the IN-IH and ME were similar, we have shown only the results of the IN-IH and refer to the region as MBH. Under both light cycles, the expression of almost all genes was rhythmic in the MBH (one-way factorial ANOVA, P < 0.05), except for Clock under both light cycles and Cry2 under short days (one-way factorial ANOVA, P > 0.05, Fig. 3Go). Per2, Per3, and Cry2 expressions peaked at ZT2, and Bmal1, Cry1, and E4bp4 expressions peaked at ZT10 under long days. Two-way factorial ANOVA failed to find any significant effect of the light conditions on the gene expression of all genes examined in the MBH (Figs. 3Go and 4Go, n = 3–6).



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  		FIG. 4. Per2 mRNA expression in the MBH, pineal gland, and SCN at ZT2 and ZT14 both under long (LD 16:8) and short days (LD 8:16).

 
The expression profile of each gene between the SCN and pineal gland was basically the same. In those structures, however, expression patterns (i.e. amplitude, phase angle, wave forms) were different between the two light conditions unlike the MBH (Figs. 3Go and 4Go). Two-way factorial ANOVA revealed significant differences in the expression of some genes between long and short days (Fig. 3Go; P < 0.05, black asterisks, n = 3–6).

Because the PT is a very small structure, it was difficult to measure the intensity of signals in most genes in this region. However, because the expression of Per2 and E4bp4 was strong enough to be measured, results of these two genes are shown (Fig. 5Go). The expression of both genes was rhythmic under both long and short days (one-way factorial ANOVA, P < 0.05, Fig. 5AGo, n = 3–6). The difference in the expression pattern between long and short days was observed in both the Per2 and E4bp4 gene (Fig. 5AGo, two-way factorial ANOVA, P < 0.01, black asterisks, n = 3–6).

Temporal expression patterns of clock genes in the MBH, SCN, and pineal gland under night interruption light schedules
It is reported that a light pulse given within the photosensitive phase induces testicular growth (21). Therefore, we next examined clock genes expression in the MBH, SCN, and pineal gland under the night interruption light schedules. Paired testes weight was significantly increased in birds exposed to a light pulse at ZT14 when compared with those at ZT7 and ZT21 (one-way factorial ANOVA, F(2,69) = 33.27, Fisher’s LSD test, asterisks P < 0.01), which indicates that ZT14 is within the photoinducible phase as in previous reports (Fig. 6Go, n = 24–25) (21).



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  		FIG. 6. Paired testes weight following three patterns of night interruption schedule for 10 d. The light pulse of 30 min were given at ZT7, ZT14, or ZT21 of LD 4:20 cycle. The weight was indicated as the mean of the paired testes weight of all animals in each group. The bar at the bottom of graph represents the light conditions. Asterisk: one-way factorial ANOVA, Fisher’s LSD test, P < 0.01. Each value is the mean + SEM (n = 24–25).

 
In the MBH, SCN, and pineal gland, the differences specific to the photoinducible phase were observed in some genes (Fig. 7Go: one-way factorial ANOVA; asterisk P < 0.05; double asterisks P < 0.01, n = 3–6). Among them, the expression of light-sensitive genes such as Per2 and Cry1 in the SCN showed two peaks only in birds exposed to a light pulse at ZT14, and expression level of Clock gene was high in the MBH and pineal gland at several time points (Fig. 7Go). Although several other differences specific to the photoinducible phase were observed in this experiment, all the differences did not coincide with the expression patterns under complete long day conditions (Figs. 3Go and 7Go). In the PT, the difference specific to the photoinducible phase was not observed on Per2 and E4bp4 expression (Fig. 5BGo).


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In the present study, we have shown different expression patterns of several clock genes in the SCN and pineal gland between long and short days (prolonged expression of Per2 and Cry1 under long days and phase angle differences of the peak time for Clock, Bmal1, and E4bp4, etc.). However, these differences were not seen under night interruption conditions. Likewise, although there were some differences between photoinducible and nonphotoinducible light cycles under night interruption conditions (two peaks of Per2 and Cry1 in the SCN, high level of Clock, etc.), they did not coincide with the patterns under the complete long and short photoperiods, respectively. Thus, there does not appear to be a unique pattern of temporal clock gene expression rhythms in the SCN and pineal gland associated with photoperiodic response. Because Per2 and Cry1 are known to be light-sensitive genes (11, 13), it is reasonable that expressions of Per2 and Cry1 are prolonged under long days and have second peak by night interruption. However, we do not have a good explanation for the different expression patterns in other genes. Although differences found in the present study are noteworthy, a lesion around the SCN or pinealectomy has no effect on the photoperiodic response of gonad in birds (22, 23). Therefore, functional significance of these differences remains to be clarified. Several groups have shown different circadian clock gene expression under different photoperiods in the SCN and/or PT of hamsters, mice, and ewes and concluded that these differences in clock gene expression may encode and decode the seasonal information in relation with the photoperiodic control of the prolactin secretion (24, 25, 26, 27, 28, 29, 30). Although our results indicated different expression patterns of clock genes under long and short days in the SCN and pineal gland, such differences were not observed in night interruption schedules. It is possible that animals may recognize seasons by different mechanisms between complete photoperiod and incomplete photoperiod (night interruption schedule). However, together with the lesion study, our results indicated that different expression patterns in the circadian pacemaker(s), the SCN and/or pineal gland are not absolute requirements for the PTM, at least in respect of the gonadal response in Japanese quail.

We have shown circadian clock gene expression in the MBH (the IN, IH, and ME). We have also confirmed endogenous expression of circadian clock genes under constant darkness and constant light in the MBH (see supplemental data published on The Endocrine Society’s Journals Online web site at http://endo.endojournals.org). This is the first demonstration of the localization of circadian clock in the MBH in which the center regulating the PTM is located. This finding seems to be particularly important because a lesion of the IN and ME blocks photoperiodic response; the immediate early gene expression is photoperiodically induced in the IN, IH, and ME; and now circadian clock, which is required for PTM, are all coincident. In addition, the IN in birds contains extraretinal photoreceptors (31, 32), which are thought to be involved in the photoperiodic light perception (33, 34). This evidence indicates that all the essential machinery for the PTM are localized in the MBH. Interestingly, although photoreceptors are localized in the MBH, expression patterns of clock genes did not appear to be affected by different light conditions. This may indicate that the photoperiodic clock in the MBH remains stable under different photoperiods enabling birds to retain information about temporal changes in light and maintain a photoinducible phase. Light pulses at the photoinducible phase seem to cause some molecular event in the MBH to secrete GnRH. Recently we succeeded in identifying a gene whose expression is induced only by a light pulse at the photoinducible phase in the MBH, and this gene seems to be responsible for the PTM (Yoshimura, T., S. Yasuo, M. Watanabe, T. Yamamura, M. Iigo, K. Hirunagi, A. Nishimura, and S. Ebihara, unpublished observations). Together with the present study, our observation might lead to understanding molecular mechanism of the PTM in birds.

Although in mammals, melatonin is a very important factor controlling the PTM, there is little evidence that melatonin controls the reproductive cycle in birds (1). Recently several researchers focused on the PT because of a great density of melatonin-binding sites in the PT (35), and some differences of the expression pattern of clock genes between long and short days in the PT have been reported (24, 26, 30). In mammals, however, melatonin acts on the PTM in two ways: One involves the regulation of prolactin secretion, and the other involves the LH. The target site of melatonin for lactotropic response is considered to be the PT (35, 36), and that for gonadotropic response is thought to be the MBH (37, 38, 39). It is known that the MBH is the target site for the melatonin action related to LH secretion in mammals (38, 40, 41). In addition, MBH lesions can block the gonadal response to the short photoperiod in Syrian hamsters (39, 42). These reports suggest that the center of mammalian photoperiodic gonadotropic responses is located in the MBH, not in the PT, in the same way as birds, and it may be important to draw attention to the MBH in mammals. The mammalian arcuate nucleus is considered to be the counter part for the avian IN. It is noteworthy that clock genes are expressed in the arcuate nucleus in mice and Syrian hamsters (43, 44). In the present study, we also observed clock gene expression in the PT of Japanese quail. Although expression patterns of Per2 under long and short days were different in the PT, this difference was not observed in night interruption light conditions. The function of these clock genes in the PT remains to be determined. Although IN lesions in Japanese quail result in the block of gonadal development under long days, these lesions do not have effects on the response of prolactin to the long photoperiod (5). Recently similar findings were reported in Syrian hamsters (42). Therefore, it is possible to speculate that the avian PT regulates prolactin secretion as in mammals and that clock gene expression in the PT may contribute to the control of prolactin secretion.

In conclusion, this study describes the expression of circadian clock genes in the SCN, pineal gland, and MBH. Although expression patterns of clock genes were different between long and short photoperiods in the SCN and pineal gland, the results were not consistent with those under night interruption schedules, which cause testicular growth. These results indicate that different expression patterns of clock genes in the circadian pacemakers are not an absolute requirement for encoding and decoding of seasonal information. In contrast, expression patterns of clock genes in the MBH were stable under various light conditions. On the basis of this evidence, we propose that the photoperiodic clock, which might be located in the MBH, enables birds to keep steady-state photoinducible phase for the PTM.


   Acknowledgments
 
We thank Nagoya University Radioisotope Center for use of facilities and Dr. T. Okano for providing cCry1 and cCry2 sequence before its availability in GenBank. We also thank Dr. Thomas Van’t Hof for helpful discussion.


   Footnotes
 
This work was supported by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN), Narishige Zoological Science Award, and Grant-in-Aid for Young Scientist from the Ministry of Education, Culture, Sports, Science, and Technology (to T.Y.) and for Scientific Research (to S.E.).

Abbreviations: IH, Inferior hypothalamic nucleus; IN, infundibular nucleus; LD, light/dark cycle; LSD, least significant difference; MBH, mediobasal hypothalamus; ME, median eminence; PT, pars tuberalis; PTM, photoperiodic time measurement; ROD, relative OD; SCN, suprachiasmatic nucleus; ZT, zeitgeber time.

Received April 8, 2003.

Accepted for publication June 9, 2003.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Gwinner E, Hau M, Heigl S 1997 Melatonin: generation and modulation of avian circadian rhythms. Brain Res Bull 44:439–444[CrossRef][Medline]
  2. Sharp PJ, Follett BK 1969 The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinology 5:205–218[Medline]
  3. Davies DT, Follett BK 1975 The neuroendocrine control of gonadotrophin release in Japanese quail. I. The role of the tuberal hypothalamus. Proc R Soc Lond B 191:285–301[Medline]
  4. Ohta M, Homma K 1987 Detection of neural connections to the infundibular complex by partial or complete hypothalamic deafferentation in male quail. Gen Comp Endocrinol 68:286–292[CrossRef][Medline]
  5. Juss TS 1993 Neuroendocrine and neural changes associated with the photoperiodic control of reproduction. In: Sharp PJ, ed. Avian endocrinology. Bristol, United Kingdom: Society for Endocrinology; 47–60
  6. Konishi H, Foster RG, Follett BK 1987 Evidence for a daily rhythmicity in the acute release of luteinizing hormone in response to electrical stimulation in the Japanese quail. J Comp Physiol A 161:315–319[CrossRef][Medline]
  7. Ohta M, Wada M, Homma K 1984 Induction of rapid testicular growth in Japanese quail by phasic electrical stimulation of the hypothalamic photosensitive area. J Comp Physiol A 154:583–589[CrossRef]
  8. Meddle SL, Follett BK 1995 Photoperiodic activation of Fos-like immunoreactive protein in neurons within the tuberal hypothalamus of Japanese quail. J Comp Physiol A 176:79–89[Medline]
  9. Meddle SL, Follett BK 1997 Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J Neurosci 17:8909–8918[Abstract/Free Full Text]
  10. Pittendrigh CS 1972 Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. Proc Natl Acad Sci USA 69:2734–2737[Abstract/Free Full Text]
  11. Yoshimura T, Suzuki Y, Makino E, Suzuki T, Kuroiwa A, Matsuda Y, Namikawa T, Ebihara S 2000 Molecular analysis of avian circadian clock genes. Mol Brain Res 78:207–215[Medline]
  12. Okano T, Yamamoto K, Okano K, Hirota T, Kasahara T, Sasaki M, Takanaka Y, Fukada Y 2001 Chicken pineal clock genes: implication of BMAL2 as a bidirectional regulator in circadian clock oscillation. Genes Cells 6:825–836[Abstract]
  13. Yamamoto K, Okano T, Fukada Y 2001 Chicken pineal Cry genes: light-dependent up-regulation of cCry1 and cCry2 transcripts. Neurosci Lett 313:13–16[CrossRef][Medline]
  14. Doi M, Nakajima Y, Okano T, Fukada Y 2001 Light-induced phase-delay of the chicken pineal circadian clock is associated with the induction of cE4bp4, a potential transcriptional repressor of cPer2 gene. Proc Natl Acad Sci USA 98:8089–8094[Abstract/Free Full Text]
  15. Chong NW, Bernard M, Klein DC 2000 Characterization of the chicken serotonin N-acetyltransferase gene. Activation via clock gene heterodimer/E box interaction. J Biol Chem 275:32991–32998[Abstract/Free Full Text]
  16. Fu Z, Inaba M, Noguchi T, Kato H 2002 Molecular cloning and circadian regulation of cryptochrome genes in Japanese quail (Coturnix coturnix japonica). J Biol Rhythms 17:14–27[Abstract/Free Full Text]
  17. Yoshimura T, Yasuo S, Suzuki Y, Makino E, Yokota Y, Ebihara S 2001 Identification of the suprachiasmatic nucleus in birds. Am J Physiol 280:R1185–R1189
  18. Wada M 1979 Photoperiodic control of LH secretion in Japanese quail with special reference to the photoinducible phase. Gen Comp Endocrinol 39: 141–149
  19. Abraham U, Albrecht U, Gwinner E, Brandstätter R 2002 Spatial and temporal variation of passer Per2 gene expression in two distinct cell groups of the suprachiasmatic hypothalamus in the house sparrow (Passer domesticus). Eur J Neurosci 16:429–436[CrossRef][Medline]
  20. Yasuo S, Yoshimura T, Bartell PA, Iigo M, Makino E, Okabayashi N, Ebihara S 2002 Effect of melatonin administration on qPer2, qPer3, and qClock gene expression in the suprachiasmatic nucleus of Japanese quail. Eur J Neurosci 16:1541–1546[CrossRef][Medline]
  21. Follett BK, Sharp PJ 1969 Circadian rhythmicity in photoperiodically induced gonadotrophin release and gonadal growth in the quail. Nature 223:968–971[Medline]
  22. Davies DT, Follett BK 1975 The neuroendocrine control of gonadotrophin release in the Japanese quail. II. The role of the anterior hypothalamus. Proc R Soc Lond B 191:303–315[Medline]
  23. Siopes TD, Wilson WO 1974 Extraocular modification of photoreception in intact and pinealectomized coturnix. Poult Sci 53:2035–2041[Medline]
  24. Messager S, Ross AW, Barrett P, Morgan PJ 1999 Decoding photoperiodic time through Per1 and ICER gene amplitude. Proc Natl Acad Sci USA 96:9938–9943[Abstract/Free Full Text]
  25. Messager S, Hazelrigg DG, Mercer JG, Morgan PJ 2000 Photoperiod differentially regulates the expression of Per1 and ICER in the pars tuberalis and the suprachiasmatic nucleus of the Siberian hamster. Eur J Neurosci 12:2865–2870[CrossRef][Medline]
  26. Nuesslein-Hildesheim B, O’Brien JA, Ebling FJP, Maywood ES, Hastings MH 2000 The circadian cycle of mPER clock gene products in the suprachiasmatic nucleus of the Siberian hamster encodes both daily and seasonal time. Eur J Neurosci 12:2856–2864[CrossRef][Medline]
  27. Daan S, Albrecht U, Horst GTJ, Illnerova H, Roenneberg T, Wehr TA, Schwartz WJ 2001 Assembling a clock for all seasons: Are there M and E oscillators in the genes? J Biol Rhythms 16:105–116[Abstract/Free Full Text]
  28. Hastings M 2001 Modeling the molecular calendar. J Biol Rhythms 16:117–123[Free Full Text]
  29. Oster H, Maronde E, Albrecht U 2002 The circadian clock as a molecular calendar. Chronobiol Int 19:507–516[CrossRef][Medline]
  30. Lincoln GA, Messager S, Andersson H, Hazlerigg D 2002 Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proc Natl Acad Sci USA 99:13890–13895[Abstract/Free Full Text]
  31. Siver R, Witkovsky P, Horvath P, Alones V, Barnstable CJ, Lehman MN 1988 Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res 253:189–198[CrossRef][Medline]
  32. Saldanha CJ, Leak RK, Silver R 1994 Detection and transduction of day length in birds. Psychoneuroendocrinology 19:641–656[CrossRef][Medline]
  33. Oliver J, Baylé JD 1982 Brain photoreceptors for the photo-induced testicular response in birds. Experientia 38:1021–1029[CrossRef][Medline]
  34. Wilson FE 1991 Neither retinal nor pineal photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea). J Exp Zool 259:117–127[CrossRef]
  35. Morgan PJ, Williams LM 1996 The pars tuberalis of the pituitary: a gateway for neuroendocrine output. Rev Reprod 1:153–161[Abstract]
  36. Lincoln GA, Clarke IJ 1995 Evidence that melatonin acts in the pituitary gland through a dopamine-independent mechanism to mediate effects of daylength on the secretion of prolactin in the ram. J Neuroendocrinol 7:637–643[CrossRef][Medline]
  37. Malpaux B, Daveau A, Maurice F, Gayrard V, Thiéry JC 1993 Short-day effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biol Reprod 48:752–760[Abstract]
  38. Malpaux B, Skinner DC, Maurice F 1995 The ovine pars tuberalis does not appear to be target by melatonin to modulate luteinizing hormone secretion, but may be important for prolactin release. J Neuroendocrinol 7:199–206[CrossRef][Medline]
  39. Maywood ES, Hastings MH 1995 Lesions of the iodomelatonin-binding sites of the mediobasal hypothalamus spare the lactotrophic, but block the gonadotrophic response of male Syrian hamsters to short photoperiod and to melatonin. Endocrinology 136:144–153[Abstract]
  40. Lincoln GA, Maeda KI 1992 Reproductive effects of placing micro-implants of melatonin in the mediobasal hypothalamus and preoptic area in rams. J Endocrinol 132:201–215[Abstract/Free Full Text]
  41. Malpaux B, Daveau A, Maurice F, Duarte G, Chemineau P 1998 Evidence that melatonin acts in the premammillary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone secretion by in situ microimplant delivery. Endocrinology 139:1508–1516[Abstract/Free Full Text]
  42. Lewis D, Freeman DA, Dark J, Wynne-Edwards KE, Zucker I 2002 Photoperiodic control of oestrous cycles in Syrian hamsters: mediation by the mediobasal hypothalamus. J Neuroendocrinol 14:294–299[CrossRef][Medline]
  43. Takumi T, Taguchi K, Miyake S, Sakakida Y, Takashima N, Matsubara C, Maebayashi Y, Okumura K, Takekida S, Yamamoto S, Yagita K, Yan L, Young MW, Okamura H 1998 A light-independent oscillatory gene mPer3 in mouse SCN and OVLT. EMBO J 17:4753–4759[CrossRef][Medline]
  44. Yamamoto S, Shigeyoshi Y, Ishida Y, Fukuyama T, Yamaguchi S, Yagita K, Moriya T, Shibata S, Takashima N, Okamura H 2001 Expression of the Per1 gene in the hamster: brain atlas and circadian characteristics in the suprachiasmatic nucleus. J Comp Neurol 430:518–532[CrossRef][Medline]



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