Exposure to an open-field arena increases c-Fos expression in a subpopulation of neurons in the dorsal raphe nucleus, including neurons projecting to the basolateral amygdaloid complex

Neuroscience

Volumn 157, Issue 4, 2008, Pages 733-748

  Hale, M W ^a   Hay Schmidt, A ^b   Mikkelsen, J D ^c   Poulsen, B ^b   Bouwknecht, J A ^e   Evans, A K ^a   Stamper, C E ^a   Shekhar, A ^d   Lowry, C A ^a,e  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Rigshospitalet   (Denmark)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

5 HT; amygdala; anxiety; basolateral nucleus; retrograde tracing

Indexed keywords

CHOLERA TOXIN B SUBUNIT; PROTEIN C FOS; TRYPTOPHAN HYDROXYLASE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CELL ACTIVATION; CELL COUNT; CELL POPULATION; COMPARATIVE STUDY; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; FOREBRAIN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MESENCEPHALON; NERVE CELL; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEROTONINERGIC SYSTEM;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CELL COUNT; CHOLERA TOXIN; EXPLORATORY BEHAVIOR; MALE; MOTOR ACTIVITY; NEURAL PATHWAYS; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RAPHE NUCLEI; RATS; RATS, WISTAR; TIME FACTORS; TRYPTOPHAN HYDROXYLASE;

EID: 56549117569     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.09.050     Document Type: Article

References (48)

1. Abrams J.K., Johnson P.L., Hay-Schmidt A., Mikkelsen J.D., Shekhar A., and Lowry C.A. Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 133 (2005) 983-997
2. Azmitia E.C. The serotonin-producing neurons of the midbrain median and dorsal raphe nuclei. In: Iversen L.L., Iversen S.H., and Snyder S.H. (Eds). Chemical pathways in the brain (1981), Plenum, New York 233-314
3. Belzung C., and Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 125 (2001) 141-149
4. Bouwknecht J.A., Spiga F., Staub D.R., Hale M.W., Shekhar A., and Lowry C.A. Differential effects of exposure to low-light or high-light open-field on anxiety-related behaviors: Relationship to c-Fos expression in serotonergic and non-serotonergic neurons in the dorsal raphe nucleus. Brain Res Bull 72 (2007) 32-43
5. Bruhwyler J. Anxiolytic potential of a microgram dose of chlordiazepoxide in the open-field test. Eur J Pharmacol 187 (1990) 547-549
6. Campbell B.M., and Merchant K.M. Serotonin 2C receptors within the basolateral amygdala induce acute fear-like responses in an open-field environment. Brain Res 993 (2003) 1-9
7. Commons K.G., Connolley K.R., and Valentino R.J. A neurochemically distinct dorsal raphe-limbic circuit with a potential role in affective disorders. Neuropsychopharmacology 28 (2003) 206-215
8. Durand M., Berton O., Aguerre S., Edno L., Combourieu I., Mormede P., and Chaouloff F. Effects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis in SHR and WKY rats. Neuropharmacology 38 (1999) 893-907
9. Gonzalez L.E., Andrews N., and File S.E. 5-HT1A and benzodiazepine receptors in the basolateral amygdala modulate anxiety in the social interaction test, but not in the elevated plus-maze. Brain Res 732 (1996) 145-153
10. Grubbs F.E. Procedures for detecting outlying observations in samples. Technometrics 11 (1969) 1-21
11. Hale M.W., Bouwknecht J.A., Spiga F., Shekhar A., and Lowry C.A. Exposure to high- and low-light conditions in an open-field test of anxiety increases c-Fos expression in specific subdivisions of the rat basolateral amygdaloid complex. Brain Res Bull 71 (2006) 174-182
12. Hale M.W., Hay-Schmidt A., Mikkelsen J.D., Poulsen B., Shekhar A., and Lowry C.A. Exposure to an open-field arena increases c-Fos expression in a distributed anxiety-related system projecting to the basolateral amygdaloid complex. Neuroscience 155 (2008) 659-672
13. Hammack S.E., Schmid M.J., LoPresti M.L., Der-Avakian A., Pellymounter M.A., Foster A.C., Watkins L.R., and Maier S.F. Corticotropin releasing hormone type 2 receptors in the dorsal raphe nucleus mediate the behavioral consequences of uncontrollable stress. J Neurosci 23 (2003) 1019-1025
14. Hard E., Engel J., Larsson K., and Musi B. Effect of diazepam, apomorphine and haloperidol on the audiogenic immobility reaction and on the open field behavior. Psychopharmacology (Berl) 85 (1985) 106-110
15. Higgins G.A., Bradbury A.J., Jones B.J., and Oakley N.R. Behavioural and biochemical consequences following activation of 5HT1-like and GABA receptors in the dorsal raphe nucleus of the rat. Neuropharmacology 27 (1988) 993-1001
16. Higgins G.A., Jones B.J., and Oakley N.R. Effect of 5-Ht1A receptor agonists in 2 models of anxiety after dorsal raphe injection. Psychopharmacology 106 (1992) 261-267
17. Hirsjarvi P.A., Junnila M.A., and Valiaho T.U. Gentled and non-handled rats in a stressful open-field situation; differences in performance. Scand J Psychol 31 (1990) 259-265
18. Janusonis S., and Fite K.V. Diurnal variation of c-Fos expression in subdivisions of the dorsal raphe nucleus of the Mongolian gerbil (Meriones unguiculatus). J Comp Neurol 440 (2001) 31-42
19. Lowry C.A., Johnson P.L., Hay-Schmidt A., Mikkelsen J.D., and Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 8 (2005) 233-246
20. Maier S.F., and Watkins L.R. Stressor controllability, anxiety, and serotonin. Cogn Ther Res 22 (1998) 595-613
21. Mascagni F., and McDonald A.J. A novel subpopulation of 5-HT type 3A receptor subunit immunoreactive interneurons in the rat basolateral amygdala. Neuroscience 144 (2007) 1015-1024
22. McDonald A.J., and Mascagni F. Neuronal localization of 5-HT type 2A receptor immunoreactivity in the rat basolateral amygdala. Neuroscience 146 (2007) 306-320
23. Mikkelsen J.D., Hay-Schmidt A., and Larsen P.J. Central innervation of the rat ependyma and subcommissural organ with special reference to ascending serotoninergic projections from the raphe nuclei. J Comp Neurol 384 (1997) 556-568
24. Muller J.F., Mascagni F., and McDonald A.J. Serotonin-immunoreactive axon terminals innervate pyramidal cells and interneurons in the rat basolateral amygdala. J Comp Neurol 505 (2007) 314-335
25. O'Connor W.T., Earley B., and Leonard B.E. Antidepressant properties of the triazolobenzodiazepines alprazolam and adinazolam: studies on the olfactory bulbectomized rat model of depression. Br J Clin Pharmacol 19 Suppl 1 (1985) 49S-56S
26. Ottersen O.P. Afferent connections to the amygdaloid complex of the rat with some observations in the cat. III. Afferents from the lower brain stem. J Comp Neurol 202 (1981) 335-356
27. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1998), Academic Press, Inc, San Diego, CA
28. Petersen R.G. Design and analysis of experiments (1985), M Dekker, New York
29. Petit J.M., Luppi P.H., Peyron C., Rampon C., and Jouvet M. VIP-like immunoreactive projections from the dorsal raphe and caudal linear raphe nuclei to the bed nucleus of the stria terminalis demonstrated by a double immunohistochemical method in the rat. Neurosci Lett 193 (1995) 77-80
30. Peyron C., Petit J.M., Rampon C., Jouvet M., and Luppi P.H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 82 (1998) 443-468
31. Prut L., and Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463 (2003) 3-33
32. Rex A., Voigt J.P., Voits M., and Fink H. Pharmacological evaluation of a modified open-field test sensitive to anxiolytic drugs. Pharmacol Biochem Behav 59 (1998) 677-683
33. Rizvi T.A., Ennis M., Behbehani M.M., and Shipley M.T. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 303 (1991) 121-131
34. Russchen F.T. Amygdalopetal projections in the cat. II. Subcortical afferent connections. A study with retrograde tracing techniques. J Comp Neurol 207 (1982) 157-176
35. Sajdyk T.J., Schober D.A., and Gehlert D.R. Neuropeptide Y receptor subtypes in the basolateral nucleus of the amygdala modulate anxiogenic responses in rats. Neuropharmacology 43 (2002) 1165-1172
36. Sajdyk T.J., Schober D.A., Gehlert D.R., and Shekhar A. Role of corticotropin-releasing factor and urocortin within the basolateral amygdala of rats in anxiety and panic responses. Behav Brain Res 100 (1999) 207-215
37. Sajdyk T.J., and Shekhar A. Excitatory amino acid receptors in the basolateral amygdala regulate anxiety responses in the social interaction test. Brain Res 764 (1997) 262-264
38. Sena L.M., Bueno C., Pobbe R.L., Andrade T.G., Zangrossi Jr. H., and Viana M.B. The dorsal raphe nucleus exerts opposed control on generalized anxiety and panic-related defensive responses in rats. Behav Brain Res 142 (2003) 125-133
39. Siemiatkowski M., Sienkiewicz-Jarosz H., Czlonkowska A.I., Bidzinski A., and Plaznik A. Effects of buspirone, diazepam, and zolpidem on open field behavior, and brain [3H]muscimol binding after buspirone pretreatment. Pharmacol Biochem Behav 66 (2000) 645-651
40. Silveira M.C., Sandner G., and Graeff F.G. Induction of Fos immunoreactivity in the brain by exposure to the elevated plus-maze. Behav Brain Res 56 (1993) 115-118
41. Silveira M.C., Zangrossi H., de Barros V., Silveira R., and Graeff F.G. Differential expression of Fos protein in the rat brain induced by performance of avoidance or escape in the elevated T-maze. Behav Brain Res 126 (2001) 13-21
42. Singewald N., Salchner P., and Sharp T. Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol Psychiatry 53 (2003) 275-283
43. Singewald N., and Sharp T. Neuroanatomical targets of anxiogenic drugs in the hindbrain as revealed by Fos immunocytochemistry. Neuroscience 98 (2000) 759-770
44. Spiga F., Lightman S.L., Shekhar A., and Lowry C.A. Injections of urocortin 1 into the basolateral amygdala induce anxiety-like behavior and c-Fos expression in brainstem serotonergic neurons. Neuroscience 138 (2006) 1265-1276
45. Staub D.R., Spiga F., and Lowry C.A. Urocortin 2 increases c-Fos expression in topographically organized subpopulations of serotonergic neurons in the rat dorsal raphe nucleus. Brain Res 1044 (2005) 176-189
46. Stein L., Wise C.D., and Belluzzi J.D. Effects of benzodiazepines on central serotonergic mechanisms. Adv Biochem Psychopharmacol (1975) 29-44
47. Stezhka V.V., and Lovick T.A. Projections from dorsal raphe nucleus to the periaqueductal grey matter: studies in slices of rat midbrain maintained in vitro. Neurosci Lett 230 (1997) 57-60
48. Van Bockstaele E.J., Biswas A., and Pickel V.M. Topography of serotonin neurons in the dorsal raphe nucleus that send axon collaterals to the rat prefrontal cortex and nucleus accumbens. Brain Res 624 (1993) 188-198