The Suprachiasmatic Nucleus in Organotypic Slice Cultures of the Common Vole ( Microtus arvalis ): Comparison of Development with Rat and Hamster and the Effect of Age
Free accessResearch articleFirst published online February, 2000
The Suprachiasmatic Nucleus in Organotypic Slice Cultures of the Common Vole ( Microtus arvalis ): Comparison of Development with Rat and Hamster and the Effect of Age
The intrinsic properties of the suprachiasmatic nucleus (SCN), the site of the main circadian pacemaker in mammals, have recently been studied in vitro by means of organotypic slice culturing. So far, only neonatal rats and mice have been used for such developmental and functional analyses of the isolated pacemaker. Here, the authors present a comparative developmental study of the SCN of voles, rats, and hamsters in organotypic slice cultures. In contrast to strictly circadian organization of behavior in rats and hamsters, common voles (Microtus arvalis) are characterized by large variability in the strength of circadian organization of behavior. It is not known to what extent this variability is reflected in the intrinsic features of the SCN. Cultures were prepared from rat, hamster, and vole pups (6 to 9 days old) for the purpose of species comparison. In addition, the authors studied the relation between age and development in cultures from pup (7 to 10 days old), juvenile (15 to 16 days old), and young adult (1 to 2 months old) voles. In contrast to the situation in rat and hamster, the most striking feature in neonatal voles is the variability in shape of the final, fully developed culture and its poor resemblance with the in vivo SCN. The SCN of adult voles, however, could be cultured successfully while retaining its morphological organization seen in situ. Phase-contrast microscopy and immunocytochemical staining for vasopressin and glial fibrillary acidic protein revealed that cultures of pup and juvenile voles still have potential for neurogenesis and morphological reorganization. Young voles, therefore, can serve as a model to study the developmental establishment of a functional circadian pacemaker, while adult voles allow the study of intrinsic pacemaker properties in relation to previously recorded behavior of the donor and aging-related pacemaker dysfunction.
Aguilar-Roblero R, Shibata S, Speh JC, Drucker-Colín R, and Moore RY (1992) Morphological and functional development of the suprachiasmatic nucleus in transplanted fetal hypothalamus. Brain Res580:288-296.
2.
Belenky M, Wagner S, Yarom Y, Matzner H, Cohen S, and Castel M (1996) The suprachiasmatic nucleus in stationary organotypic culture. Neuroscience70:127-143.
3.
Boer GJ and Griffioen HA (1990) Development and functional aspects of grafting of the suprachiasmatic nucleus in the Brattleboro and the arrhythmic rat. Eur J Morphol28:330-345.
4.
del Rio JA, Heimrich B, Soriano E, Schwegler H, and Frotscher M (1991) Proliferation and differentiation of glial fibrillary acidic protein-immunoreactive glial cells in organotypic slice cultures of rat hippocampus. Neuroscience43:335-347.
5.
Gähwiler BH (1984) Slice cultures of cerebellar, hippocampal and hypothalamic tissue. Experientia40:235-243.
6.
Gähwiler BH, Capogna M, Debanne D, McKinney RA, and Thompson SM (1997) Organotypic slice cultures: A technique has come of age. Trends Neurosci20:471-477.
7.
Gerkema MP, Daan S, Wilbrink M, Hop MW, and van der Leest F (1993) Phase control of ultradian feeding rhythms in the common vole (Microtus arvalis): The role of light and the circadian system. J Biol Rhythms7:151-171.
8.
Gerkema MP, Groos GA, and Daan S (1990) Differential elimination of circadian and ultradian rhythmicity by hypothalamic lesions in the common vole, Microtus arvalis. J Biol Rhythms5:81-95.
9.
Gerkema MP, Shinohara K, and Kimura F (1999) Lack of circadian patterns in vasoactive intestinal peptide release and variability in vasopressin release in vole suprachiasmatic nuclei in vitro. Neurosci Lett259:107-110.
10.
Gerkema MP, Van der Zee EA, and Feitsma LE (1994) Expression of circadian rhythmicity correlates with the number of arginine-vasopressin-immunoreactive cells in the suprachiasmatic nucleus of common voles, Microtus arvalis. Brain Res639:93-101.
11.
Honma S, Katsuno Y, Tanahashi Y, Abe H, and Honma K (1998) Circadian rhythms of arginine vasopressin and vasoactive intestinal polypeptide do not depend on cytoarchitecture of dispersed cell culture of rat suprachiasmatic nucleus. Neuroscience86:967-976.
12.
House SB, Thomas A, Kusano K, and Gainer H (1998) Stationary organotypic cultures of oxytocin and vasopressin magnocellular neurons from rat and mouse hypothalamus. J Neuroendocrinol10:849-861.
13.
Jansen K, Van der Zee EA, and Gerkema MP (1998) Concurrent decrease of vasopressin and protein kinase C[.alpha] immunoreactivity during the light phase in the vole suprachiasmatic nucleus. Neurosci Lett248:81-84.
14.
Jansen K, Van der Zee EA, and Gerkema MP (2000) Organotypic suprachiasmatic nuclei cultures of adult voles reflect locomotor behavior: Differences in number of vasopressin cells. Chronobiol Int16:745-750.
15.
Kawahara F, Saito H, and Katsuki H (1994) Primary culture of postnatal rat suprachiasmatic neurons in serum-free supplemented medium. Brain Res651:101-107.
16.
Kuhn HG, Dickinson-Anson H, and Gage FHJ (1996) Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J Neurosci16:2027-2033.
17.
Lavialle M and Serviere J (1995) Developmental study in the circadian clock of the golden hamster: A putative role of astrocytes. Dev Brain Res86:275-282.
18.
Madeira MD, Andrade JP, Lieberman AR, Sousa N, Almeida OIX, and Paula-Barbosa MM (1997) Chronic alcohol consumption and withdrawal do not induce cell death in the suprachiasmatic nucleus, but lead to irreversible depression of peptide immunoreactivity and mRNA levels. J Neurosci17:1302-1319.
Okamura H, Tominaga K, Ban Y, Fukuhara C, Yanaihara N, Ibata Y, and Inouye S-IT (1994a) Morphological survey of the suprachiasmatic nucleus in slice culture using roller tube method: 2. Peptidergic neurons. Acta Histochem Cytochem27:171-179.
21.
Okamura H, Tominaga K, Ban Y, Tanaka M, Tamada Y, Inouye S-IT, and Ibata Y (1994b) Morphological survey of the suprachiasmatic nucleus in slice culture using roller tube method: 1. Architecture of the suprachiasmatic nucleus in vitro. Acta Histochem Cytochem27:159-169.
22.
Prosser RA, Edgar DM, Heller HC, and Miller JD (1994) A possible glial role in the mammalian circadian clock. Brain Res643:296-301.
23.
Ralph MR, Foster RG, Davis FC, and Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science247:975-978.
24.
Rickmann M, Amaral DG, and Cowan WM (1987) Organization of radial glial cells during the development of the rat dentate gyrus. J Comp Neurol264:449-479.
25.
Ridet JL, Malhotra SK, Privat A, and Gage FH (1997) Reactive astrocytes: Cellular and molecular cues to biological function. Trends Neurosci20:570-577.
26.
Romero MT, Lehman MN, and Silver R (1993) Age of donor influences ability of suprachiasmatic nucleus grafts to restore circadian rhythmicity. Dev Brain Res71:45-52.
27.
Shinohara K, Honma S, Katsuno Y, Abe H, and Honma K (1994) Circadian rhythms in the release of vasoactive intestinal polypeptide and arginine-vasopressin in organotypic slice culture of rat suprachiasmatic nucleus. Neurosci Lett170:183-186.
28.
Shinohara K, Honma S, Katsuno Y, Abe H, and Honma K (1995) Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc Natl Acad Sci USA92:7396-7400.
29.
Shinohara K, Honma S, Katsuno Y, Abe H, and Honma K (1998) Circadian release of amino acids in the suprachiasmatic nucleus in vitro. Neuroreport9:137-140.
30.
Silver R, Lehman MN, Gibson M, Gladstone WR, and Bittman EL (1990) Dispersed cell suspensions of fetal SCN restore circadian rhythmicity in SCN-lesioned adult hamsters. Brain Res525:45-58.
31.
Tamada Y, Tanaka M, Munekawa K, Hayashi S, Okamura H, Kubo T, Hisa Y, and Ibata Y (1998) Neuron-glia interaction in the suprachiasmatic nucleus: A double labeling light and electron microscopic immunocytochemical study in the rat. Brain Res Bull45:281-287.
32.
Tominaga K, Geusz ME, Michel S, and Inouye S-IT (1994a) Calcium imaging in organotypic cultures of the rat suprachiasmatic nucleus. Neuroreport5:1901-1905.
33.
Tominaga K, Inouye S-IT, and Okamura H (1994b) Organotypic slice culture of the rat suprachiasmatic nucleus: Sustenance of cellular architecture and circadian rhythm. Neuroscience59:1025-1042.
34.
Tominaga K, Okamura H, and Inouye S-IT (1994c) Organo-typic slice culture of the suprachiasmatic nucleus. Neurosci Biobehav Rev18:601-604.
35.
Tominaga K, Shinohara K, Otori Y, Fukuhara C, and Inouye S-IT (1992) Circadian rhythms of vasopressin content in the suprachiasmatic nucleus of the rat. Neuroreport3:809-812.
36.
Van der Zee EA, Jansen K, and Gerkema MP (1999) Severe loss of vasopressin-immunoreactive cells in the suprachiasmatic nucleus of aging voles coincides with reduced circadian organization of running wheel activity. Brain Res816:572-579.
37.
Van der Zee EA, Naber PA, and Disterhoft JF (1997) Age-dependent changes in the immunoreactivity for neurofilaments in rabbit hippocampus. Neuroscience79:103-116.
38.
Wollnik F and Bihler S (1996) Strain differences in the distribution of arginine-vasopressin-and neuropeptide Y-immunoreactive neurons in the suprachiasmatic nucleus of laboratory rats. Brain Res724:191-199.
39.
Wray S, Castel M, and Gainer H (1993) Characterization of the suprachiasmatic nucleus in organotypic slice explant cultures. Microsc Res Tech25:46-60.
