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Effect of chronic variable stress on corticosterone levels and hippocampal extracellular 5-HT in rats with persistent differences in positive affectivity

Published online by Cambridge University Press:  24 June 2014

Karita Raudkivi ,
Tanel Mällo  and
Jaanus Harro
Karita Raudkivi
Affiliation:
Department of Psychology, Estonian Centre of Behavioural and Health Sciences, University of Tartu, Tiigi 78, 50410, Tartu, Estonia
Tanel Mällo
Affiliation:
Department of Psychology, Estonian Centre of Behavioural and Health Sciences, University of Tartu, Tiigi 78, 50410, Tartu, Estonia
Jaanus Harro*
Affiliation:
Department of Psychology, Estonian Centre of Behavioural and Health Sciences, University of Tartu, Tiigi 78, 50410, Tartu, Estonia
*
Professor Jaanus Harro, Department of Psychology, Estonian Centre of Behavioural and Health Sciences, University of Tartu, Tiigi 78, 50410, Tartu, Estonia. Tel: +3727375902; Fax: +3727376152; E-mail: jaanus.harro@ut.ee
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Extract

Objective: The trait of experiencing positive affect could make a unique contribution to the pathogenesis of affective disorders. Animal models of positive emotionality are scarce but 50-kHz ultrasonic vocalizations (USVs) in rats have been associated with rewarding experience. We have previously reported that persistent inter-individual differences in expression of 50-kHz USVs (chirps) exist, and that male rats producing fewer 50-kHz USVs are more sensitive to chronic variable stress (CVS). In this study we examined the effect of CVS on extracellular serotonin (5-HT) levels in hippocampus, comparing high-chirping (HC) and low-chirping (LC) rats.

Methods: Male rats were classified as HC- and LC-rats on the basis of stable levels of USV response using sessions of tickling-like stimulation. CVS procedure lasted 4 weeks. The administration of citalopram (1 μM) and measurements of levels of 5-HT were done by microdialysis. Corticosterone levels were also measured from trunk blood.

Results: Male LC-rats were more sensitive to CVS: the effect of stress on body weight gain was larger and corticosterone levels from full blood were higher in the stressed LC animals as compared to both the unstressed groups and the stressed HC animals. While no baseline differences in extracellular 5-HT levels in hippocampus were found between groups, the increase in extracellular 5-HT levels induced by citalopram was much higher in LC-rats.

Conclusion: Chronic stress appears to modify hippocampal 5-HT overflow in rats with low positive affectivity. This finding supports the notion of greater vulnerability to CVS in male rats with low positive affectivity.

Keywords

chronic variable stressdepressionpositive affectserotoninultrasonic vocalization

Information

Type
Research Article
Information
Acta Neuropsychiatrica , Volume 24 , Issue 4 , August 2012 , pp. 208 - 214
Copyright
Copyright © Cambridge University Press 2011

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References

1.Singewald, N.Altered brain activity processing in high-anxiety rodents revealed by challenge paradigms and functional mapping. Neurosci Biobehav Rev 2007;31:18–40. DOI: 10.1016/j.neubiorev.2006.02.003.Google Scholar
2.Harro, J.Inter-individual differences in neurobiology as vulnerability factors for affective disorders: Implications for psychopharmacology. Pharmacol Ther 2010;125:402–422.CrossRefGoogle ScholarPubMed
3.Clark, LA, Watson, D.Tripartite model of anxiety and depression: psychometric evidence and taxonomic implications. J Abnorm Psychol 1991;100:316–336. DOI: 10.1037/0021-843X.100.3.316.Google Scholar
4.Forbes, EE, Dahl, RE.Neural systems of positive affect: relevance to understanding child and adolescent depression? Dev Psychopathol 2005;17:827–850. DOI: 10.1017/S095457940505039X.Google Scholar
5.Fredrickson, BL.What good are positive emotions? Rev Gen Psychol 1998;2:300–319.Google Scholar
6.Fredrickson, BL.The role of positive emotions in positive psychology. The broaden-and-build theory of positive emotions. Am Psychol 2001;56:218–226. DOI: 10.1037//0003-066X.56.3.218.Google Scholar
7.Geschwind, N, Nicolson, NA, Peeters, F, Os, J, Barge-schaapveld, D, Wichers, M.Early improvement in positive rather than negative emotion predicts remission from depression after pharmacotherapy. Eur Neuropsychopharmacol 2011;21:241–247. DOI: 10.1016/j.euroneuro.2010.11.004.Google Scholar
8.Tellegen, A. Structures of mood and personality and their relevance to assessing anxiety, with an emphasis on self-report. In Tuma, AH and Maser, JD, eds. Anxiety and the anxiety disorders, Hillsdale: Erlbaum, 1985: 681–706.Google Scholar
9.Gross, JJ, John, OP.Individual differences in two emotion regulation processes: Implications for affect, relationships, and well-being. J Pers Soc 2003;85:348–362. DOI: 10.1037/0022-3514.85.2.348.CrossRefGoogle ScholarPubMed
10.Panksepp, J.Neuroevolutionary sources of laughter and social joy: modeling primal human laughter in laboratory rats. Behav Brain Res 2007;182:231–244. DOI: 10.1016/j.bbr.2007.02.015.Google Scholar
11.Sale, G, Pye, D.Ultrasonic communication by animals. London: Chapman and Hall, 1974.Google Scholar
12.Miczek, KA, Tornatzky, W, Vivian, J. Ethology and neuro–pharmacology: Rodent ultrasounds. In Olivier, B, Mos, J, Slangen, JL, eds. Animal models in psychopharmacology. Boston: Birkhauser Verlag, 1991:409–427.CrossRefGoogle Scholar
13.Blanchard, RJ, Blanchard, DC, Agullana, R, Weiss, SM.Twenty two kHz alarm cries to presentations of a predator, by laboratory rats living in visible burrow systems. Physiol Behav 1991;50:967–972. DOI: 10.1016/0031-9384(91)90423-L.CrossRefGoogle ScholarPubMed
14.Vivian, JA, Miczek, KA.Ultrasound during morphine withdrawal in rats. Psychopharmacology 1991;104:187–193. DOI: 10.1007/BF02244177.CrossRefGoogle ScholarPubMed
15.Sanchez, C.Stress-induced vocalization in adult animal: a valid model of anxiety? Eur J Pharmacol 2003;463:133–143. DOI: 10.1016/S0014-2999(03)01277-9.Google Scholar
16.Tonoue, T, Ahida, Y, Makino, H, Hata, H.Inhibition of shock-elicited ultrasonic vocalization by opioid peptides in the rat: a psychotropic effect. Psychoneuroendocrinology 1986;1:177–184. DOI: 10.1016/0306-4530(86)90052-1.Google Scholar
17.Knutson, B, Burgdorf, J, Panksepp, J.High-frequency ultrasonic vocalizations index conditioned pharmacological reward in rats. Physiol Behav 1999;66:639–643. DOI: 10.1016/S0031-9384(98)00337-0.CrossRefGoogle ScholarPubMed
18.Panksepp, J, Burgdorf, J.Laughing rats and the evolutionary antecedents of human joy? Physiol Behav 2003;79:533–547. DOI: 10.1016/S0031-9384(03)00159-8.CrossRefGoogle ScholarPubMed
19.Burgdorf, J, Panksepp, J.Tickling induces reward in adolescent rats. Physiol Behav 2001;72:167–173. DOI: 10.1016/S0031-9384(00)00411-X.CrossRefGoogle ScholarPubMed
20.Burgdorf, J, Panksepp, J, Brudzynski, SM, Kroes, R, Moskal, JR.Breeding for 50-kHz positive affective vocalization in rats. Behav Genet 2005;35:67–72. DOI: 10.1007/s10519-004-0856-5.Google Scholar
21.Panksepp, J, Knutson, B, Burgdorf, J.The role of brain emotional systems in addictions: a neuro-evolutionary perspective and new “self-report” animal model. Addiction 2002;97:459–469. DOI: 10.1046/j.1360-0443.2002.00025.x.Google Scholar
22.Gilmer, WS, Mckinney, WT.Early experience and depressive disorders: human and non-human primate studies. J Affect Disord 2003;75:97–113. DOI: 10.1016/S0165-0327(03)00046-6.Google Scholar
23.Katz, RJ, Roth, KA, Carroll, BJ.Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neurosci Biobehav Rev 1981;5:247–251. DOI: 10.1016/0149-7634(81)90005-1.Google Scholar
24.Katz, RJ.Animal model of depression: pharmacological sensitivity of a hedonic deficit. Pharmacol Biochem Behav 1982;16:965–968. DOI: 10.1016/0091-3057(82)90053-3.Google Scholar
25.Zurita, A, Cuadra, G, Molina, VA.The involvement of an opiate mechanism in the sensitized behavior deficit induced by early chronic variable stress: Influence of desipramine. Behav Brain Res 1999;110:153–159.Google Scholar
26.Willner, P.Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005;52:90–110. DOI: 10.1159/000087097.Google Scholar
27.Millan, MJ.The neurobiology and control of anxious states. Prog Neurobiol 2003;70:83–244. DOI: 10.1016/ S0301-0082(03)00087-X.Google Scholar
28.Morilak, DA, Frazer, A.Antidepressants and brain monoaminergic systems: a dimensional approach to understanding their behavioural effects in depression and anxiety disorders. Int J Neuropsychopharmacol 2004;7:193–218. DOI: 10.1017/S1461145704004080.CrossRefGoogle ScholarPubMed
29.File, SE, Kenny, PJ, Cheeta, S.The role of the dorsal hippocampal serotonergic and cholinergic systems in the modulation of anxiety. Pharmacol Biochem Behav 2000;66:65–72. DOI: 10.1016/S0091-3057(00)00198-2.Google Scholar
30.Joels, M, Karst, H, Alfarez, D et al. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004;7:221–231.Google Scholar
31.Mckittrick, CR, Blanchard, DC, Blanchard, RJ, McEwen, BS, Sakai, RR.Serotonin receptor binding in a colony model of chronic social stress. Biol Psychiatry 1995; 37:383–393.Google Scholar
32.Mällo, T, Matrov, D, Herm, L et al. Tickling-induced 50-kHz ultrasonic vocalization is individually stable and predicts behaviour in tests of anxiety and depression in rats. Behav Brain Res 2007;184:57–71. DOI: 10.1016/j.bbr.2007.06.015.Google Scholar
33.Mällo, T, Matrov, D, Kõiv, K, Harro, J.Effect of chronic stress on behavior and cerebral oxidative metabolism in rats with high or low positive affect. Neuroscience 2009;164:963–974. DOI: 10.1016/j.neuroscience.2009.08.041.Google Scholar
34.Harro, J, Tõnissaar, M, Eller, M, Kask, A, Oreland, L.Chronic variable stress and partial 5-HT denervation by parachloroamphetamine treatment in the rat: effects on behavior and monoamine neurochemistry. Brain Res 2001; 899:227–239. DOI: 10.1016/S0006-8993(01)02256-9.Google Scholar
35.Mällo, T, Kõiv, K, Koppel, I et al. Regulation of extracellular serotonin levels and brain-derived neurotrophic factor in rats with high and low exploratory activity. Brain Res 2008;1194:110–117. DOI: 10.1016/j.brainres.2007.11.041.Google Scholar
36.Paxinos, G, Watson, C.The rat brain in stereotaxic coordinates. San Diego: Academic Press, 1986.Google Scholar
37.Thorre, K, Ebinger, G, Michotte, Y.5-HT4 receptor involvement in the serotonin-enhanced dopamine efflux from the substantia nigra of the freely moving rat: a microdialysis study. Brain Res 1998;796:117–124. DOI: 10.1016/S0006-8993(98)00337-0.Google Scholar
38.Bosker, FJ, Cremers, TIFH, Jongsma, ME, Westerink, BHC, Wikstrom, HV, Boer, JA.Acute and chronic effects of citalopram on postsynaptic 5-hydroxytryptamine1A receptor-mediated feedback: a microdialysis study in the amygdala. J Neurochem 2001;76:1645–1653. DOI: 10.1046/j.1471-4159.2001.00194.x.Google Scholar
39.Moreau, JL, Jenck, F, Martin, JR, Mortas, P, Haefely, WE.Antidepressant treatment prevents chronic unpredictable mild stress-induced anhedonia as assessed by ventral tegmentum self-stimulation in rats. Eur Neuropsychopharmacol 1992;2:43–49. DOI: 10.1016/0924-977X(92)90035-7.Google Scholar
40.Nielsen, CK, Arnt, J, Sanchez, C.Intracranial self-stimulation and sucrose intake differ as hedonic measures following chronic mild stress: interstrain and interindividual differences. Behav Brain Res 2000;107:21–33. DOI: 10.1016/S0166-4328(99)00110-2.Google Scholar
41.Willner, P, Moreau, JL, Nielsen, CK, Papp, M, Sluzewska, A.Decreased hedonic responsiveness following chronic mild stress is not secondary to loss of body weight. Physiol Behav 1996;60:129–134. DOI: 10.1016/0031-9384(95)02256-2.Google Scholar
42.Harro, J, Häidkind, R, Harro, M et al. Chronic mild unpredictable stress after noradrenergic denervation: attenuation of behavioural and biochemical effects of DSP-4 treatment. Eur Neuropsychopharmacol 1999;10:5–16. DOI: 10.1016/S0924-977X(99)00043-7.Google Scholar
43.Blakely, RD, DE Felice, LJ, Hartzell, HC.Molecular physiology of norepinephrine and serotonin transporters. J Exp Biol 1994;196:263–281.CrossRefGoogle ScholarPubMed
44.Lesch, KP, Gutknecht, L.Pharmacogenetics of the serotonin transporter. Prog Neuropsychopharmacol Biol Psychiatry 2005;29:1062–1073. DOI: 10.1016/j.pnpbp.2005.03.012.Google Scholar
45.Jennings, KA, Loder, MK, Sheward, WJ et al. Increased expression of the 5-HT transporter confers a low-anxiety phenotype linked to decreased 5-HT transmission. J Neurosci 2006;26:8955–8964. DOI: 10.1523/JNEUROSCI.5356-05.2006.CrossRefGoogle ScholarPubMed
46.Wellman, CL, Izquierdo, A, Garrett, JE et al. Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci 2007;27:684–691. DOI: 10.1523/JNEUROSCI.4595-06.2007.CrossRefGoogle ScholarPubMed
47.Moret, C, Briley, M.The possible role of 5-HT1B/D receptors in psychiatric disorders and their potential as a target for therapy. Eur J Pharmacol 2000;404:1–12. DOI: 10.1016/S0014-2999(00)00581-1.Google Scholar
48.Harro, J, Oreland, L.Depression as a spreading adjustment disorder of monoaminergic neurons: a case for primary implication of the locus coeruleus. Brain Res Rev 2001; 38:79–128. DOI: 10.1016/S0165-0173(01)00082-0.Google Scholar
49.Curzon, G.5-Hydroxytryptamine and corticosterone in an animal model of depression. Prog Neuro-Psychopharmacol Biol Psychiat 1989;13:305–310. DOI: 10.1016/0278-5846(89)90119-X.Google Scholar
50.Abelson, KSP, Adem, B, Royo, F, Carlsson, HE, Hau, J.High plasma corticosterone levels persist during frequent automatic blood sampling in rats. In Vivo 2005;19:815–819.Google Scholar