Global Depletion of Dopamine Using Intracerebroventricular 6-hydroxydopamine Injection Disrupts Normal Circadian Wheel-running Patterns and PERIOD2 Expression in the Rat Forebrain

Overview

Journal J Mol Neurosci

Specialties Molecular Biology
Neurology

Date 2011 Apr 13

PMID 21484443

Citations 37

Authors

Luciana Gravotta

Alex M Gavrila

Suzanne Hood

Shimon Amir

Affiliations

Soon will be listed here.

Abstract

Normal circadian rhythms of behavior are disrupted in disorders involving the dopamine (DA) system, such as Parkinson's disease. We have reported previously using unilateral injections of the catecholamine toxin, 6-hydroxydopamine (6-OHDA), into the medial forebrain bundle that DA signaling regulates daily expression of the clock protein, PERIOD2 (PER2), in the dorsal striatum of the rat. In the present study, we made widespread lesions of DA fibers using large injections of 6-OHDA into the third ventricle to determine the involvement of DA in normal daily rhythms of wheel-running activity and PER2 patterns in the suprachiasmatic nucleus (SCN) and several regions of the limbic forebrain. Rats injected with 6-OHDA and housed in constant darkness were less active in the wheel and showed a disorganized pattern of activity in which wheel running was not confined to a specific phase over 24 h. The 6-OHDA injection had no effect on the daily PER2 pattern in the SCN, but blunted the normal rise in PER2 in the dorsal striatum. 6-OHDA also blunted PER2 expression in the periventricular nucleus of the hypothalamus, a region in which a daily PER2 pattern has not been previously reported in male rats, and in the oval nucleus of the bed nucleus of the stria terminalis, but not in the central nucleus of the amygdala. These results indicate that DA plays a prominent role in regulating circadian activity at both behavioral and molecular levels.

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References

Lamont E, Robinson B, Stewart J, Amir S . The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc Natl Acad Sci U S A. 2005; 102(11):4180-4. PMC: 554834. DOI: 10.1073/pnas.0500901102. View

Amir S, Lamont E, Robinson B, Stewart J . A circadian rhythm in the expression of PERIOD2 protein reveals a novel SCN-controlled oscillator in the oval nucleus of the bed nucleus of the stria terminalis. J Neurosci. 2004; 24(4):781-90. PMC: 6729822. DOI: 10.1523/JNEUROSCI.4488-03.2004. View

Gunn D, Naismith S, Lewis S . Sleep disturbances in Parkinson disease and their potential role in heterogeneity. J Geriatr Psychiatry Neurol. 2010; 23(2):131-7. DOI: 10.1177/0891988709358591. View

Davis M, Walker D, Lee Y . Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. Philos Trans R Soc Lond B Biol Sci. 1998; 352(1362):1675-87. PMC: 1692102. DOI: 10.1098/rstb.1997.0149. View

Rosenblad C, Kirik D, Devaux B, Moffat B, PHILLIPS H, Bjorklund A . Protection and regeneration of nigral dopaminergic neurons by neurturin or GDNF in a partial lesion model of Parkinson's disease after administration into the striatum or the lateral ventricle. Eur J Neurosci. 1999; 11(5):1554-66. DOI: 10.1046/j.1460-9568.1999.00566.x. View

Amir S, Robinson B . Thyroidectomy alters the daily pattern of expression of the clock protein, PER2, in the oval nucleus of the bed nucleus of the stria terminalis and central nucleus of the amygdala in rats. Neurosci Lett. 2006; 407(3):254-7. DOI: 10.1016/j.neulet.2006.08.057. View

Imbesi M, Yildiz S, Dirim Arslan A, Sharma R, Manev H, Uz T . Dopamine receptor-mediated regulation of neuronal "clock" gene expression. Neuroscience. 2008; 158(2):537-44. PMC: 3664916. DOI: 10.1016/j.neuroscience.2008.10.044. View

Lamont E, Harbour V, Barry-Shaw J, Renteria Diaz L, Robinson B, Stewart J . Restricted access to food, but not sucrose, saccharine, or salt, synchronizes the expression of Period2 protein in the limbic forebrain. Neuroscience. 2006; 144(2):402-11. DOI: 10.1016/j.neuroscience.2006.09.027. View

Segall L, Amir S . Exogenous corticosterone induces the expression of the clock protein, PERIOD2, in the oval nucleus of the bed nucleus of the stria terminalis and the central nucleus of the amygdala of adrenalectomized and intact rats. J Mol Neurosci. 2010; 42(2):176-82. DOI: 10.1007/s12031-010-9375-4. View

10.

Ben V, Bruguerolle B . Effects of bilateral striatal 6-OHDA lesions on circadian rhythms in the rat: a radiotelemetric study. Life Sci. 2000; 67(13):1549-58. DOI: 10.1016/s0024-3205(00)00751-7. View

11.

Cai Y, Liu S, Sothern R, Xu S, Chan P . Expression of clock genes Per1 and Bmal1 in total leukocytes in health and Parkinson's disease. Eur J Neurol. 2009; 17(4):550-4. DOI: 10.1111/j.1468-1331.2009.02848.x. View

12.

Ramanathan C, Nunez A, Martinez G, Schwartz M, Smale L . Temporal and spatial distribution of immunoreactive PER1 and PER2 proteins in the suprachiasmatic nucleus and peri-suprachiasmatic region of the diurnal grass rat (Arvicanthis niloticus). Brain Res. 2006; 1073-1074:348-58. DOI: 10.1016/j.brainres.2005.11.082. View

13.

Spanagel R, Pendyala G, Abarca C, Zghoul T, Sanchis-Segura C, Magnone M . The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption. Nat Med. 2004; 11(1):35-42. DOI: 10.1038/nm1163. View

14.

Alheid G, Heimer L . New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience. 1988; 27(1):1-39. DOI: 10.1016/0306-4522(88)90217-5. View

15.

Perrin J, Segall L, Harbour V, Woodside B, Amir S . The expression of the clock protein PER2 in the limbic forebrain is modulated by the estrous cycle. Proc Natl Acad Sci U S A. 2006; 103(14):5591-6. PMC: 1459398. DOI: 10.1073/pnas.0601310103. View

16.

Gonzalez S, Scorticati C, Garcia-Arencibia M, de Miguel R, Ramos J, Fernandez-Ruiz J . Effects of rimonabant, a selective cannabinoid CB1 receptor antagonist, in a rat model of Parkinson's disease. Brain Res. 2006; 1073-1074:209-19. DOI: 10.1016/j.brainres.2005.12.014. View

17.

Thompson R, Swanson L . Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res Brain Res Rev. 2003; 41(2-3):153-202. DOI: 10.1016/s0165-0173(02)00232-1. View

18.

Hood S, Cassidy P, Cossette M, Weigl Y, Verwey M, Robinson B . Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J Neurosci. 2010; 30(42):14046-58. PMC: 6634752. DOI: 10.1523/JNEUROSCI.2128-10.2010. View

19.

Boulamery A, Simon N, Vidal J, Bruguerolle B . Effects of L-Dopa on circadian rhythms of 6-OHDA striatal lesioned rats: a radiotelemetric study. Chronobiol Int. 2010; 27(2):251-64. DOI: 10.3109/07420521003664213. View

20.

Bruguerolle B, Simon N . Biologic rhythms and Parkinson's disease: a chronopharmacologic approach to considering fluctuations in function. Clin Neuropharmacol. 2002; 25(4):194-201. DOI: 10.1097/00002826-200207000-00002. View