Effects of hypothalamic lesions on the ultradian and circadian organization of wheel running and feeding were studied in the common vole, Microtus arvalis. Circadian organization broke down within 30 days in continuous darkness in 24% of intact voles (n = 135). Ultradian rhythmicity of feeding (period 2-3 hr) persisted in constant conditions in all intact voles.
Following lesions of the suprachiasmatic nuclei (SCN), circadian rhythmicity disappeared when lesions were complete (n = 8) or more extensive than 25% of the total SCN volume (n = 5). Absence of circadian rhythmicity was also found in animals with substantial lesions in the diencephalic paraventricular area (PVA) and in the retrochiasmatic area (RCA) and/or adjacent arcuate nucleus (Arc). Complete loss of ultradian and circadian organization occurred in eight voles with damage to the RCA and/or Arc. In three of these, the SCN was intact.
The SCN is a likely candidate for a circadian pacemaker in voles (as in other rodents), while the loss of circadian rhythmicity following PVA and RCA/Arc lesions may be due to destruction of efferent pathways from the SCN. The RCA/Arc area is apparently necessary for the expression of ultradian rhythms. The intact SCN is neither necessary nor sufficient for the generation of ultradian rhythmicity.
References
1.
Albers, H.E., R. Lydic, P.H. Gander, and M.C. Moore-Ede (1981) Gradual decay of circadian drinking organization following lesions of the suprachiasmatic nuclei in primates. Neurosci. Lett.69: 47-52.
2.
Aschoff, J. (1962) Spontane Lokomotorische Aktivitdt. In Handbuch der Zoologie, J. G. Helmcke, H. v. Lengerken, and D. Starck , eds., Vol. 8, Section 11(4), pp. 1-76, de Gruyter, Berlin.
3.
Aschoff, J., and M.P. Gerkema (1985) On diversity and uniformity of ultradian rhythms . Exp. Brain Res. (Suppl. 12): 321-334.
4.
Berk, M.L., and J.A. Finkelstein (1981) An autoradiographic determination of the efferent projections of the suprachiasmatic nucleus of the hypothalamus . Brain Res.226: 1-13.
5.
Boulos, Z., A.M. Rosenwasser, and M. Terman (1980) Feeding schedules and the circadian organization of behavior in the rat. Behav. Brain Res.I: 39-65.
6.
Buttner, D., and F. Wollnik (1984) Strain-differentiated circadian and ultradian rhythms in locomotor activity of the laboratory rat. Behav. Genet.14: 137-152.
7.
Chronwall, B.M. (1985) Anatomy and physiology of the neuroendocrine arcuate nucleus. Peptides6: 1-11.
8.
Daan, S. (1987) Clocks and hourglasses in behavioural cycles. In Comparative Aspects of Circadian Clocks, T. Hiroshige and K. I. Honma, eds., pp. 42-58, Hokkaido University Press, Sapporo.
9.
Daan, S., and S. Slopsema (1978) Short-term rhythms in foraging behavior in the common vole, Microtus arvalis. J. Comp. Physiol. A127: 215-227.
10.
Eastman, C.I., R.E. Mistlberger, and A. Recht-Schaffen (1984) Suprachiasmatic nuclei lesions eliminate circadian temperature and sleep rhythms in the rat. Physiol. Behav.32: 357-368.
11.
Gerkema, M.P., and S. Daan (1985) Ultradian rhythms in behavior: The case of the common vole (Microtus arvalis). Exp. Brain Res. (Suppl. 12): 11-31.
12.
Groos, G.A. (1984) The physiological organization of the circadian sleep-wake cycle. Exp. Brain Res. (Suppl. 8): 241-257.
13.
Honma, K.L., and T. Hiroshige (1978) Endogenous ultradian rythms in rats exposed to prolonged continuous light. Am. J. Physiol.235: R250-R256.
14.
Honma, K.I., and S. Honma (1985) Ultradian rhythms in locomotor activity, deep body temperature and plasma corticosterone levels in rats: Two different origins ? Exp. Brain Res. (Suppl. 12): 77-94.
15.
Honma, S., K.I. Honma, and T. Hiroshige (1984) Dissociation of circadian rhythms in rats with a hypothalamic island. Am. J. Physiol.246: R949-R954.
16.
Hoogenboom, I., S. Daan, J.H. Dallinga, and M. Schoenmakers (1984) Seasonal change in the daily timing of behaviour of the common vole, Microtus arvalis. Oecologia61: 18-31.
17.
Inouye, S. (1983) Does the ventromedial hypothalamic nucleus contain a self-sustained circadian oscillator associated with periodic feeding? Brain Res.279: 53-63.
18.
Inouye, S., and H. Kawamura (1982) Characteristics of a circadian pacemaker in the suprachiasmatic nuclei. J. Comp. Physiol. A 146: 153-160.
19.
Kawakami, M., T. Uemura, and R. Hayashi (1982) Electrophysiological correlates of pulsatile gonadotropin release in rats. Neuroendocrinology35: 63-67.
20.
Kenagy, G.J., and D. Vleck (1982) Daily temporal organization of metabolism in small mammals: Adaptation and diversity. In Vertebrate Circadian Systems, J. Aschoff, S. Daan, and G. A. Groos , eds., pp 322-338, Springer-Verlag, Berlin.
21.
Kimura, F., and C.W. Tsai (1984) Ultradian rhythm of growth hormone secretion and sleep in the adult male rat. J. Physiol. ( London) 353: 305-315.
22.
Kleitman, N., and T.G. Engelmann (1953) Sleep characteristics of infants. J. Appl. Physiol.6: 269-282.
23.
Knobil, E. (1980) Neuroendocrine control of the menstrual cycle. Rec. Prog. Horm. Res.36: 53-58.
24.
Konig, J.F. , and R.A. Klippel (1963) The Rat Brain: A Stereotaxic Atlas of the Forebrain and Lower Parts of the Brain Stem, Williams & Wilkins , Baltimore.
25.
Le Magnen, J. (1981) The metabolic basis of dual periodicity of feeding in rats. Behav. Brain Sci.4: 561-607.
26.
Madison, D.M. (1985) Activity rhythms and spacing. In Biology of New World Microtus, American Society of Mammalogists Special Publication No. 8, R. H. Tamarin, ed., pp. 373-419, American Society of Mammalogists, Shippensburg, PA .
27.
Martin, J.B. (1979) Brain mechanisms for integration of growth hormone secretion. Physiologist22: 23-29.
28.
Meijer, J.H., and W.J. Rietveld (1989) The neurophysiology of the suprachiasmatic circadian pacemaker in rodents. Physiol. Rev.69: 671-707.
29.
Mistlberger, R.E., and B. Rusak (1988) Food-anticipatory circadian rhythms in rats with paraventricular and lateral hypothalamic ablations. J. Biol. Rhythms3: 277-291.
30.
Mosier, H.D., and R.A. Jansons (1987) Lack of synchrony between feeding activity and pulsatile growth hormone secretion in rats. Physiol. Behav.39: 183-185.
31.
Nelson, K. (1965) After-effects of courtship in the male three-spined stickleback. Z. Vergl. Physiol.50: 569 -597.
32.
Pickard, G.E. (1982) The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection . J. Comp. Neurol.211: 65-83.
33.
Pickard, G.E., and F.W. Turek (1983) The hypothalamic paraventricular nucleus mediates the photoperiodic control of reproduction but not the effects of light on the circadian rhythm of activity. Neurosci. Lett.43: 67-72.
34.
Pickard, G.E., and F.W. Turek (1985) Effects of partial destruction of the suprachiasmatic nuclei on two circadian parameters: Wheel-running activity and short-day induced testicular regression. J. Comp. Physiol. A 156: 803-815.
35.
Richter, C.P. (1980) Growth hormone 3.6-h pulsatile secretion and feeding times have similar periods in rats. Am. J. Physiol.239: E1-E2.
36.
Rietveld, W.J., M. Koou, W. Flory, and O.R. Aar-Doom (1982) The effect of dorsomedial hypothalamic nucleus lesions on the circadian control of food intake, locomotor activity, body temperature and estrous cycle in rats. IRCS-Biochem.10: 905-906.
37.
Rusak, B. (1989) The mammalian circadian system: Models and physiology . J. Biol. Rhythms4: 121-134.
38.
Rusak, B., and I. Zucker (1979) Neural regulation of circadian rhythms. Physiol. Rev.59: 449-526.
39.
Sidman, R.L., J.B. Angevine, and E.T. Pierce (1971) Atlas of the Mouse Brain and Spinal Cord, Harvard University Press, Cambridge, MA.
40.
Slotnick, B.M., and C.M. Leonard (1975) A Stereotaxic Atlas of the Albino Mouse Forebrain , DHEW Publication No. ADM 75-100, U.S. Government Printing Office, Washington, DC.
41.
Sokolove, P.G., and W.N. Bushell (1978) The chisquare periodogram: Its utility for analysis of circadian rhythms. J. Theor. Biol.74: 131-160.
42.
Stephan, F.K., K.J. Berkley, and R.L. Moss (1981) Efferent connections of the rat suprachiasmatic nucleus. Neuroscience6: 2625-2641.
43.
Stephan, F.K., and I. Zucker (1972) Circadian rhythms in drinking behavior and locomotor activity are eliminated by hypothalamic lesions. Proc. Natl. Acad. Sci. USA69: 1583-1586.
44.
Van Den Pol, A.N., and T. Powley (1979) A fine-grained anatomical analysis of the role of the rat suprachiasmatic nucleus in circadian rhythms of feeding and drinking . Brain Res.160: 307-326.
45.
Watts, A.G., L.W. Swanson, and G. Sanchez-Watts (1987) Efferent projections of the suprachiasmatic nucleus : I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J. Comp. Neurol.258: 204- 229.
46.
Wehrenberg, W.B., P. Brazeau, R. Luben, P. Bohlen, and R. Guillemin (1982) Inhibition of the pulsatile secretion of growth hormone by monoclonal antibodies to the hypothalamic growth hormone releasing factor (GRF). Endocrinology111: 2147-2148.
47.
Weingarten, H.P., P. Chang, and T.J. McDonald (1985) Comparison of the metabolic and behavioral disturbances following paraventricular and ventromedial hypothalamic lesions. Brain Res. Bull.14: 551-559.
