This post was originally written on February 11, 2005. Moving from relatively simple mammalian model to more complex systems.
I have previously described the basic properties of the circadian organization in mammals. Non-mammalian vertebrates (fish, amphibians, reptiles and birds) have more complex circadian systems than mammals. While the suprachiasmatic area remains a site of circadian pacemakers, it is, unlike in mammals, not the only such site.
The pineal organ, which in mammals is a purely secretory organ, is directly photosensitive in other vertebrates (with the exception of snakes) and is a site of a circadian pacemaker. Retinae of the eyes are also sites of circadian pacemakers in at least some non-mammalian vertebrates. Extra-retinal photoreceptors that can mediate entrainment of circadian clocks are also found deep inside the brain.
Thus, the non-mammalian circadian system is composed of multiple pacemakers (eyes, pineal, SCN) and multiple photic inputs (eyes, pineal, deep-brain photoreceptors). These structures communicate with each other neurally and humorally and provide a single synchronized output in the rhythmic behavior of the animal.
However, the properties and relative importance of each structure can differ between species. For instance, pinealectomy has different effects in different species of lizards, leading to either splitting (left), arrhythmicity (middle),or period-change (right)(from Underwood, 1977):
While research has been done in lampreys, some fish, frogs, and lizards, most of the work on non-mammalian vertebrates has been conducted in birds. I will return, in the future, to more detailed reviews of chronobiology of other vertebrate classes, but today, I will concentrate on birds.
Birds (click for a review)
The circadian system of birds involves several components: a central hypothalamic clock (SCN), the pineal organ, the retinae and extraretinal photoreceptors. These elements show different degrees of involvement in the production of the circadian output in different avian species. Some components (such as the SCN and pineal, or the eyes and the SCN) may be coupled together via the hormone, melatonin.
In house sparrows, the pineal is the master pacemaker of the circadian system and pinealectomy results in complete arrhythmicity. In European starling, pinealectomy can result in period change or arrhythmicity, depending on the individual. In pigeons, neither blinding alone nor pinealectomy alone disrupts circadian rhythms, yet removal of both the pineal and the eyes results in complete arrhythmicity.
There is some controversy concerning which hypothalamic nucleus in birds is the homologue of the mammalian SCN. Classical anatomical studies suggest that the avian SCN resides adjacent to the preoptic recess of the third ventricle and the optic chiasm in the nucleus termed the “medial hypothalamic nucleus” (MHN), also sometimes referred to as the “periventricular preoptic nucleus” (PPN) whereas studies of the termination of the retinohypothalamic tract (RH) suggest that the SCN resides more caudally, between the supraoptic decussations and the vLGN, in a nucleus termed the “lateral hypothalamic retinorecipient nucleus” (LHRN), also termed the “visual SCN”. However, a number of studies in birds, including cholera toxin mapping of retinal projections in pigeons, show that both the MHN and the LHRN can receive significant retinal input. Immunohistochemical analyses of the various neurochemicals and neurotransmitters could not demonstrate complete homology between the mammalian SCN and either MHN or the LHRN.
Several investigators have lesioned the MHN of birds to determine if these lesions would lead to loss of rhythmicity in the locomotor activity of animals held in continuous darkness (DD), but the total number of species (or individuals) examined is small and, in some cases, the lesions may also have damaged the LHRN as well. Arrhythmicity is caused by MNH lesions in Java sparrows, Japanese quail and house sparrows. In house sparrows, it is the LHRN which shows a circadian rhythm of metabolic activity as measured by 2-deoxy[14C]glucose uptake. This rhythm is abolished by pinealectomy and restored by daily melatonin injections. In pigeons, lesions of either of the two nuclei did not abolish rhythmicity, although some disruptions of the activity rhythm could be seen. In chicks, lesions of the LHRN abolished the circadian rhythm of epinephrine turnover in the pineal, while the lesions of the MHN had no effect. Recent data on expression of RNA for the clock genes in Japanese quail, Java sparrow, chicken and pigeon suggest the MHN as the locus of the circadian pacemaker, although these studies were performed either in immature males or the sex of the animals was not reported, thus leaving open the possibility that the LHRN may have a function in ovulating females. In the house sparrow, however, circadian expression of the clock gene per was observed in both the MHN and the LHRN, but the sex, age and reproductive status of these individuals were not noted.
It is likely that the central clocks in birds are, themselves, multioscillator in nature: that is, each “clock” in the suprachiasmatic area is composed of a number of interacting (coupled) circadian oscillators. Recent studies in mammals have shown that a number of individual neurons within the SCN are capable of expressing circadian rhythms of electrical activity. Furthermore, the period of the behavioral rhythm of locomotor activity in mammals is correlated with the average period of the rhythms of electrical activity expressed by individual SCN neurons. It is safe to assume for now that the SCN in non-mammalian vertebrates has similar properties.
Next time, I will go into details of the circadian organization of one avian species as an example of a non-mammalian vertebrate.