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Have you ever wondered how storks know that it is time to leave your chimney and start their long trip to South? You probably thought of the daily changes in the quantity of light, the fall in temperature, and such things. But what happens to the migrating birds when they are near to the Equator where the environment is quite stable throughout the year, or the weather can change so dramatically day by day that it can not give a reliable clue? What happens in the brain and what changes do appear when the days are getting longer? And what are the behavioral consequences of having this system impaired? Biological rhythms related to the regular daily and yearly environmental changes (circadian and circannual rhythms) are very important for the organization of the behavior and physiology of all higher organisms. Such rhythms are created within cells containing special "molecular clockwork". Those cells form the unit called "biological clock". In mammals the circadian clock is well known and appears to be in the hypothalamic suprachiasmatic nuclei (SCN). In birds the circadian pacemaking system is more complex; the avian circadian rhythms are regulated not only by the SCN, other components including the pineal gland and the retina also contributes to the generation of the circadian rhythm. Many scientists are trying to figure out why this complexity developed and how this system functions in the bird’s daily life.

Comparison with the mammalian clock:

The mammalian clock seems to be relatively simple comparing the avian clock. In mammals no other structure besides the SCN has yet been identified as containing a circadian oscillator. Photic input to the SCN is received just from the retina; whereas in birds the assumed SCN-equivalent region receives information from pineal and deep encephalic photoreceptors too. The most remarkable difference is that while the mammalian clock concentrates to one, well-defined region (the SCN), birds have three autonomous and anatomically distinct circadian clocks. The pineal contains autonomous circadian oscillator, which produces melatonin in a rhythmic manner. This is supported by the fact that avian pineal cells continue to secrete melatonin even in vitro and in the absence of light. Avian retina had been shown to produce melatonin rhythmically too, but it is not released into the bloodstream in all species. This multioscillatory organization of the circannual pacemaking system can be found in lower vertebrates too. That indicates that the highly concentrated mammalian system is quite unique and might be developed via reduction from the scattered original system.

Localization of the suprachiasmatic nucleus in birds:

In birds the exact localization of the suprachiasmatic nucleus is still disputed. Yoshimura et al. recently came up with a possible solution to decide the position of the circadian oscillator. Two possible candidates for the SCN were proposed previously: the so-called medial SCN (mSCN) and the visual SCN (vSCN). The mSCN is located near the angle of the preoptic recess of the third ventricle, while the vSCN is slightly more lateral and caudal to the mSCN. Several findings supported the vSCN to be a better candidate for the avian SCN. Those experiments showed mostly anatomical similarities between the mammalian and avian structures, like the investigation of the retinohypothalamic projections (retinohypothalamic tract=RHT) and immunocytochemical studies. On the other hand, it was shown later that the mSCN receives also projections from the retina via the RHT, and lesions of the mSCN resulted in disrupted circadian rhythm in several species, although the reason might be that because of the close anatomical location there is a high chance that the lesions included the vSCN too. The most functional approach seemed to be the determination of the expression of circadian clock genes, such as "period" and "clock", which are expressed only in known circadian oscillators in mammals. The presence of those genes in a brain region can be determined with in situ hybridization. Yoshimura and al. cloned three circadian clock genes in Japanese quail and used the in situ hybridization technique. They found in quails that the qClock ("quail" Clock), qPer2 and qPer3 genes are expressed in the mSCN but not present in the vSCN. They also showed that after pinealectomy and removing the eyes the birds still show circadian rhythmicity during continuous light conditions. That supported the existence of the encephalic photoreceptors and the hypothalamic oscillator system. The residual rhythmicity disappeared in birds that received mSCN lesion too, suggesting that the mSCN is the avian equivalent for the mammalian SCN. Other anatomical experiments showed that the vSCN receives the majority of the retinohypothalamic projections while mSCN receives just very small retinal projection. It is likely that the vSCN is not functioning as an oscillator because of the absence of the clock genes, but it might have an information conveying function to the mSCN. It is still not understood how the light information is forwarded to the mSCN. There might be a retinal projection to the mSCN that is not described yet, or the vSCN can transfer the information to the mSCN via undefined neural connections. Since the mSCN does not seem to contain melatonin receptors, it can not be regulated by the pineal gland.

Interaction of the components of avian circadian pacemaking system:

The avian pineal, like in mammals is connected to the SCN via a polysynaptic neural pathway. Several experiments showed that the interruption of this pathway disturbs the rhythm of melatonin production in the pineal gland. This suggests that the hypothalamic oscillator is involved in driving the rhythm in the pineal gland. On the other hand, the pineal should have an effect on the hypothalamic oscillator. This idea was supported by the facts that the presumed SCN contains melatonin-biding sites, and in house sparrow pinealectomy resulted in decrease of 2-deoxyglucose uptake in certain hypothalamic areas.

The other component of the avian circadian pacemaking system is the retina itself; in birds the retina produces melatonin rhythmically, just like the pineal gland, although in some species it does not seem to be crucial.

Gwinner and Brandstätter offer a model for describing the mechanism in passerine birds. They suggest that at least the hypothalamic oscillator and the pineal gland has mainly enhancing effects on each other and those two oscillators stabilize and amplify each other by resonance. Therefore the elimination of the amplitude of one of the components of the system results in the reduction of the amplitude of the other component. This model is called "The internal resonance model".

Avian species differ in the role of the eyes in the generation of the circadian rhythm and in the relative contribution of the pineal gland. In sparrows and some finches the pineal gland appears to be dominating. In those birds pinealectomy usually eliminates rhythmicity completely. In an other passerine bird, the starling, pinealectomy does not result in total elimination of the circadian rhythm, in most individuals it just destabilizes it. However, in the pigeon and the quail pinealectomy has no effect at all. In the other hand, the barn owl has a well-developed circadian system, which does not seem to depend on either the pineal gland or its periodic melatonin secretion, because in this species the pineal organ is rudimentary, and only traces of melatonin are found in the blood. The presence of this high degree of diversity among avian species in the role of the individual components of the pacemaking system is still unexplained. I assume that in those species that have a thin skull like the sparrow and other smaller birds the pineal gland can play a more significant role in the generation of circadian rhythms, since it can admit a higher quantity of the light and can receive more reliable information from the daily environmental changes than in the species having thick skull like the owl, the pigeon and other relatively big birds. There might be also an evolutionary and ecological reason; the complexity of bird clocks may be related to the diversity of the various lifestyles and environments birds evolved in, but since we have information of the circadian pacemaking system from just a very few species yet, we can not get to a reliable conclusion regarding this matter.

Avian migration and other behaviour-ecological aspects:

Photoperiodic control of seasonality:

Birds need to use their circannual rhythm to make sure that the seasonal events like breeding and song production happens in the appropriate time of the year. In species living close to the Equator these mechanisms is even more important, because the birds should rely on their inner clock more since the environmental clues are less conspicuous. In opportunistic species where the breeding might occur in different times of the year depending on the food resources, the reproductive system remains in a state of "readiness to breed" for a large part of the year

Migration:

Somehow birds know when to start migrating. The environmental clues (changes in the weather and the duration of daylight) together with the inner circannual clock results in a good timing. The role of the inner clock varies among species according to the different environment they adaped to. It was shown in migrating birds that during migratory seasons the amplitude of the 24-hour melatonin rhythm is reduced. Garden warblers are normally day active but they migrate at night. If they are kept in cages under laboratory conditions they develop intense nocturnal activity during the migration seasons. At that time the daily increase of the plasma melatonin at night is significantly smaller than in the non-migrating seasons when the birds are exclusively diurnal. It is still unknown why and how this decline occurs in the melatonin rhythm. One possible explanation might be that weakening the circadian system could be beneficial to migratory birds; it would let to a faster resynchronization and adjustment to the changing conditions the bird needs to face during the long migration across time zones. Therefore, the avian circadian pacemaking system might be able to change its properties due to endogenous factors or in response to environmental conditions, and this might be a chance for better coping with the changing environment.

Winter in non-migratory birds:

Gwinner and his group made several researches in non-migratory birds too. House sparrows were investigated in 4 periods of the year: in the time of increasing photoperiod in spring, during the longest day length in early summer, around the equinox in autumn and during the shortest photoperiod in winter. They found significant differences in the melatonin amplitude levels. Amplitudes were highest in spring and summer, intermediate in autumn and lowest in winter. The reason of this decreased amplitude might be that the system is more passive in the winter and can more readily respond to increasing day lengths in late winter and early spring.

Summary:

Although the research on the avian clock was very intense in the last few years there are still many questions unanswered. Our knowledge is highly incomplete in an evolutionary approach, since just a few species had been investigated yet. Study of different species in a comparative aspect could be an interesting field to move on with understanding the biological clock.
 
 
 
 
 
 
 
 
 
 
 
 

References:

1. Dawson, A., King, V.M., Bentley, G.E. and Ball, G.F. 2001. Photoperiodic control of seasonality in birds. J. Biol. Rhythms. 16(4):365-80. {Abstract}
2. Gwinner, E., Schwabl-Benzinger, I., Schwabl, H. and Dittami, J. 1993. Twenty-four hour melatonin profiles in a nocturnally migrating bird during and between migratory seasons. Gen. Comp. Endocrinol. 90(1):119-124. {Abstract}
3. Gwinner, E. and Brandstatter, R. 2001. Complex bird clocks. Phil. Trans. R. Soc. Lond. 356:1801-1810. {Abstract}
4. Gwinner, E., Hau, M. and Heigl, S. 1997. Melatonin: generation and modulation of avian circadian rhythms. Brain Res. Bulletin 44(4):439-444. {Abstract}
5. Korf, H.W. 1994. The pineal organ as a component of the biological clock. Phylogenic and ontogenetic considerations. Ann. NY. Acad. Sci. 719:13-42. {Abstract}
6. Nichelmann, M., Hochel, J. and Tzschentke, B. 1999. Biological rhythms in birds – development, insights and perspectives. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 124(4):429-437. {Abstract}
7. Norgren, R.B.Jr. and Silver, R. 1989. Retinohypothalamic projections and the suprachiasmatic nucleus in birds. Brain Behav. Evol. 34(2):73-83. {Abstract}
8. Yoshimura, T., Yasuo, S., Suzuki, Y., Makino, E., Yokota, Y. and Ebihara, S. 2001. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 280:R1185-R1189. {Abstract}{Full text}

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