Dual modes of extracellular serotonin changes in the rat ventral striatum modulate adaptation to a social stress environment, studied with wireless voltammetry

Experimental Brain Research

Volumn 230, Issue 4, 2013, Pages 583-596

  Nakazato, Taizo ^a  

^a JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Accumbens; Anxiety; Habituation; Obsessive compulsive disorder; Serotonin; Social stress

Indexed keywords

CITALOPRAM; DOPAMINE; SEROTONIN; SEROTONIN UPTAKE INHIBITOR;

ADAPTATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; CORPUS STRIATUM; CORRELATION ANALYSIS; DRUG MECHANISM; HABITUATION; MALE; NONHUMAN; POTENTIOMETRY; PRIORITY JOURNAL; RAT; SEROTONIN BRAIN LEVEL; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; SOCIAL INTERACTION; SOCIAL STRESS; WIRELESS VOLTAMMETRY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANXIETY; BASAL GANGLIA; BEHAVIOR, ANIMAL; DOPAMINE; EXTRACELLULAR SPACE; MALE; RATS; RATS, WISTAR; SEROTONIN; SEROTONIN UPTAKE INHIBITORS; STRESS, PHYSIOLOGICAL;

EID: 84885602913     PISSN: 00144819     EISSN: 14321106     Source Type: Journal    
DOI: 10.1007/s00221-012-3168-7     Document Type: Article

References (82)

1. Agnesi F, Tye SJ, Bledsoe JM, Griessenauer CJ, Kimble CJ, Sieck GC, Bennet KE, Garris PA, Blaha CD, Lee KH (2009) Wireless Instantaneous Neurotransmitter Concentration System-based amperometric detection of dopamine, adenosine, and glutamate for intraoperative neurochemical monitoring. J Neurosurg 111:701-711
2. Arrojo M, Baca-Garcia E, Perez-Rodriguez MM, Dolengevich-Segal H, Navio-Acosta M, Rodriguez-Salgado B, Saiz-Ruiz J (2007) Platelet monoamine oxidase activity in obsessive-compulsive disorder. Eur Psychiatry 22:525-529
3. Ballaz SJ, Akil H, Watson SJ (2007a) The 5-HT7 receptor: role in novel object discrimination and relation to novelty-seeking behavior. Neuroscience 149:192-202
4. Ballaz SJ, Akil H, Watson SJ (2007b) Analysis of 5-HT6 and 5-HT7 receptor gene expression in rats showing differences in novelty-seeking behavior. Neuroscience 147:428-438
5. Barnett SA (1975) The rat: a study in behavior. The University Chicago Press, Chicago
6. Cespuglio R, Sarda N, Gharib A, Faradji H, Chastrette N (1986) Differential pulse voltammetry in vivo with working carbon fiber electrodes: 5-hydroxyindole compounds or uric acid detection? Exp Brain Res 64:589-595
7. Chamberlain SR, Menzies L, Hampshire A, Suckling J, Fineberg NA, del Campo N, Aitken M, Craig K, Owen AM, Bullmore ET, Robbins TW, Sahakian BJ (2008) Orbitofrontal dysfunction in patients with obsessive-compulsive disorder and their unaffected relatives. Science 321(5887):421-422
8. Clarke HF, Walker SC, Crofts HS, Dalley JW, Robbins TW, Roberts AC (2005) Prefrontal serotonin depletion affects reversal learning but not attentional set shifting. J Neurosci 25:532-538
9. Crespi F (2010a) Is a divergent central serotonergic activity responsible for either despair or learning behavior in intact Wistar or Sprague-Dawley CD rats, respectively? A Concomitant behavioral and electrochemical analysis. Psychology 1:209-219
10. Crespi F (2010b) Wireless in vivo voltammetric measurements of neurotransmitters in freely behaving rats. Biosens Bioelectron 25:2425-2430
11. Crespi F, Sharp T, Maidment N, Marsden CA (1983) Differential pulse voltammetry in vivo, evidence that the uric acid contributes to the indole oxidation peak. Neurosci Lett 43:203-207
12. Crespi F, Martin KF, Marsden CA (1988) Nafion coated carbon fibre electrodes combined with differential pulse voltammetry measure 5HT release in vivo. Neuroscience 27:885-896
13. Crespi F, Dalessandro D, Annovazzi-Lodi V, Heidbreder C, Norgia M (2004) In vivo voltammetry: from wire to wireless measurements. J Neurosci Meth 140:153-161
14. Cronholm B, Asberg M, Montgomery S, Schalling D (1977) Suicidal behaviour syndrome with low CSF 5-HIAA. Br Med J 6063:776
15. Cummings JL (1993) Frontal-subcortical circuits and human behavior. Arch Neurol 50:873-880
16. De Leonibus E, Verheij MM, Mele A, Cools A (2006) Distinct kinds of novelty processing differentially increase extracellular dopamine in different brain regions. Eur J Neurosci 23:1332-1340
17. 2C receptors. Neuropharmacol 39:1114-1117
18. Di Giovanni G, Esposito E, Di Matteo V (2010) Role of serotonin in central dopamine dysfunction. CNS Neurosci Ther 16:179-194
19. Di Matteo V, Pierucci M, Esposito E, Crescimanno G, Benigno A, Di Giovanni G (2008) Serotonin modulation of the basal ganglia circuitry: therapeutic implication for Parkinson's disease and other motor disorders. Prog Brain Res 172:423-463
20. Doya K (2002) Metalearning and neuromodulation. Neural Network 15:1-24
21. Durand M, Berton O, Aguerre S, Edno L, Combourieu I, Mormède P, Chaouloff F (1999) Effects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis in SHR and WKY rats. Neuropharmacol 38:893-907
22. Fujii N, Hihara S, Nagasaka Y, Iriki A (2009) Social state representation in prefrontal cortex. Soc Neurosci 4:73-84
23. Garris PA, Ensman R, Poehlman J, Alexander A, Langley PE, Sandberg SG, Greco PG, Wightman RM, Rebec GV (2004) Wireless transmission of fast-scan cyclic voltammetry at a carbon-fiber microelectrode: proof of principle. J Neurosci Meth 140:103-115
24. Goldstein LE, Rasmusson AM, Bunney BS, Roth RH (1996) Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J Neurosci 16:4787-4798
25. Goodman WK, Foote KD, Greenberg BD, Ricciuti N, Bauer R, Ward H, Shapira NA, Wu SS, Hill CL, Rasmussen SA, Okun MS (2010) Deep brain stimulation for intractable obsessive compulsive disorder: pilot study using a blinded, staggered-onset design. Biol Psychiatry 67:535-542
26. Hajós-Korcsok E, Robinson DD, Yu JH, Fitch CS, Walker E, Merchant KM (2003) Rapid habituation of hippocampal serotonin and norepinephrine release and anxiety-related behaviors, but not plasma corticosterone levels, to repeated footshock stress in rats. Pharmacol Biochem Behav 74:609-616
27. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89-125
28. Hoffman BB (2006) Therapy of hypertension. In: Brunton L, Lazo JS, Parker K (eds) Goodman & Gilman's the pharmacological basis of therapeutics, 11th edn. McGraw-Hill, New York, pp 845-868
29. Hoffman AF, Gerhardt GA (1998) In vivo electrochemical studies of dopamine clearance in the rat substantia nigra: effects of locally applied uptake inhibitors and unilateral 6-hydroxydopamine lesions. J Neurochem 70:179-189
30. Huff W, Lenartz D, Schormann M, Lee SH, Kuhn J, Koulousakis A, Koulousakis A, Mai J, Daumann J, Maarouf M, Klosterkötter J, Sturm V (2010) Unilateral deep brain stimulation of the nucleus accumbens in patients with treatment-resistant obsessive-compulsive disorder: outcomes after one year. Clin Neurol Neurosurg 112:137-143
31. Insel TR, Mueller EA, Alterman I, Linnoila M, Murphy DL (1985) Obsessive-compulsive disorder and serotonin: is there a connection? Biol Psychiatry 20:1174-1188
32. Jenike MA, Hyman S, Baer L, Holland A, Minichiello WE, Buttolph L, Summergrad P, Seymour R, Ricciardi J (1990) A controlled trial of fluvoxamine in obsessive-compulsive disorder: implications for a serotonergic theory. Am J Psychiatry 147:1209-1215
33. Joel D, Doljansky J, Roz N, Rehavi M (2005) Role of the orbital cortex and of the serotonergic system in a rat model of obsessive compulsive disorder. Neuroscience 130:25-36
34. Kagohashi M, Nakazato T, Yoshimi K, Moizumi S, Hattori N, Kitazawa S (2008) Wireless voltammetry recording in unanesthetised behaving rats. Neurosci Res 60:120-127
35. Kawagoe R, Takikawa Y, Hikosaka O (1998) Expectation of reward modulates cognitive signals in the basal ganglia. Nature Neurosci 1:411-416
36. Kawahara Y, Kawahara H, Kaneko F, Tanaka M (2007) Long-term administration of citalopram reduces basal and stress-induced extracellular noradrenaline levels in rat brain. Psychopharmacology (Berl) 194:73-81
37. Kieran N, Ou X-M, Iyo AH (2010) Chronic social defeat downregulates the 5-HT1A receptor but not Freud-1 or NUDR in the rat prefrontal cortex. Neurosci Lett 469:380-388
38. Kirby LG, Lucki I (1998) The effect of repeated exposure to forced swimming on extracellular levels of 5-hydroxytryptamine in the rat. Stress 2:251-263
39. Kiyatkin EA, Stein EA (1994) Biphasic changes in mesolimbic dopamine signal during cocaine self-administration. NeuroReport 5:1005-1008
40. Klein E, Zohar J, Geraci MF, Murphy DL, Uhde TW (1991) Anxiogenic effects of m-CPP in patients with panic disorder: comparison to caffeine's anxiogenic effects. Biol Psychiatry 30:973-984
41. Kosofsky BE, Molliver ME (1987) The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1:153-168
42. Krotewicz M, Romaniuk A (1995) Social interactions in cats: regional brain monoamine distribution in dominant and submissive cats. Acta Neurobiol Exp 55:271-279
43. Lapiz MD, Fulford A, Muchimapura S, Mason R, Parker T, Marsden CA (2003) Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci Behav Physiol 33:13-29
44. Larson ET, Summers CH (2001) Serotonin reverses dominant social status. Behav Brain Res 121:95-102
45. Lidberg L, Belfrage H, Bertilsson L, Evenden MM, Asberg M (2000) Suicide attempts and impulse control disorder are related to low cerebrospinal fluid 5-HIAA in mentally disordered violent offenders. Acta Psychiatr Scand 101:395-402
46. Louilot A, Le Moal M, Simon H (1986) Differential reactivity of dopaminergic neurons in the nucleus accumbens in response to different behavioral situations. An in vivo voltammetric study in free moving rats. Brain Res 397:395-400
47. Lowry CA (2002) Functional subset of serotonergic neurones: implications for control of the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 14:911-923
48. Lucas LR, Celen Z, Tamashiro KLK, Blanchard RJ, Blanchard DC, Markham C, Sakai RR, Mcewen S (2004) Repeated exposure to social stress has long-term effects on indirect markers of dopaminergic activity in brain regions associated with motivated behavior. Neuroscience 124:449-457
49. Maia TV, Cooney RE, Peterson BS (2008) The neural bases of obsessive-compulsive disorder in children and adults. Dev Psychopathol 20:1251-1283
50. Mancini C, Ameringen MV (1996) Paroxetine in social phobia. J Clin Psychiatry 57:519-522
51. McCracken CB, Grace AA (2007) High-frequency deep brain stimulation of the nucleus accumbens region suppresses neuronal activity and selectively modulates afferent drive in rat orbitofrontal cortex in vivo. J Neurosci 27:12601-12610
52. McGuire PK, Bench CJ, Frith CD, Marks IM, Frackowiak RS, Dolan RJ (1994) Functional anatomy of obsessive-compulsive phenomena. Br J Psychiatry 164:459-468
53. Mitchell SN, Thomas PJ (1988) Effect of restraint stress and anxiolytic on 5-HT turnover in rat brain. Pharmacology 37:105-113
54. Nakahara D, Nakamura M (1999) Differential effect of immobilization stress on in vivo synthesis rate of monoamines in medial prefrontal cortex and nucleus accumbens of conscious rats. Synapse 32:238-242
55. Nakazato T (2005) Striatal dopamine release in the rat during a cued lever-press task for food reward and the development of changes over time measured using high-speed voltammetry. Exp Brain Res 166:137-146
56. Nakazato T, Akiyama A (1997) In vivo electrochemical measurement of the long-lasting release of dopamine and serotonin induced by intrastriatal kainic acid. J Neurochem 69:2039-2047
57. Nakazato T, Akiyama A (1998) Immediate and long-term effects of 5,7-dihydroxytryptamine on rat striatal serotonergic neurons measured by in vivo voltammetry. Neurochem Res 23:1-6
58. Nakazato T, Akiyama A (1999) High-speed voltammetry: dual measurement of dopamine and serotonin. J Neurosci Meth 89:105-110
59. Nakazato T, Akiyama A (2002) Behavioral activity and stereotypy in rats induced by L-DOPA metabolites: a possible role in the adverse effects of chronic L-DOPA treatment of Parkinson's disease. Brain Res 930:134-142
60. Nazar M, Siemiatkowski M, Członkowska A, Sienkiewicz-Jarosz H, Płaźnik A (1999) The role of the hippocampus and 5-HT/GABA interaction in the central effects of benzodiazepine receptor ligands. J Neural Transm 106:369-381
61. Nielen MM, Veltman DJ, de Jong R, Mulder G, den Boer JA (2002) Decision making performance in obsessive compulsive disorder. J Affect Disord 69:257-260
62. O'Neill RD, Gonzalez-Mora J-L, Boutelle MG, Ormonde DE, Lowry JP, Duff A, Fumero B, Fillenz M, Mas M (1991) Anomalously high concentrations of brain extracellular uric acid detected with chronically implanted probes: implications for in vivo sampling techniques. J Neurochem 57:22-29
63. Oyama G, Yoshimi K, Natori S, Chikaoka Y, Ren YR, Funayama M, Shimo Y, Takahashi R, Nakazato T, Kitazawa S, Hattori N (2010) Impaired in vivo dopamine release in parkin knockout mice. Brain Res 1352:214-222
64. Paul ED, Hale MW, Lukkes JL, Valentine MJ, Sarchet DM, Lowry CA (2011) Repeated social defeat increases reactive emotional coping behavior and alters functional responses in serotonergic neurons in the rat dorsal raphe nucleus. Physiol Behav 104:272-282
65. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, Sydney
66. Raleigh MJ, McGuire MT, Brammer GL, Pollack DB, Yuwiler A (1991) Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res 559:181-190
67. Richardson NR, Gratton A (1996) Behavior-relevant changes in nucleus accumbens dopamine transmission elicited by food reinforcement: an electrochemical study in rat. J Neurosci 16:8160-8169
68. Robinson DL, Heien ML, Wightman RM (2002) Frequency of dopamine concentration transients increases in dorsal and ventral striatum of male rats during introduction of conspecifics. J Neurosci 22:10477-10486
69. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27
70. Schultz W (2001) Reward signalling by dopamine neurons. Neuroscientist 7:293-302
71. Schulz B, Fendt M, Schnitzler HU (2002) Clonidine injections into the lateral nucleus of the amygdala block acquisition and expression of fear-potentiated startle. Eur J Neurosci 15:151-157
72. Seki Y, Aonuma H, Kanzaki R (2005) Pheromone processing center in the protocerebrum of bombyx mori revealed by nitric oxide-induced anti-cGMP immunocytochemistry. J Comp Neurol 481:340-351
73. Spigset O (1999) Adverse reactions of selective serotonin reuptake inhibitors: reports from a spontaneous reporting system. Drug Saf 20:277-287
74. Takahashi H, Takada Y, Nagai N, Urano T, Takada A (1998) Extracellular serotonin in the striatum increased after immobilization stress only in the nighttime. Behav Brain Res 91:185-191
75. Targum SD, Marshall LE (1989) Fenfluramine provocation of anxiety in patients with panic disorder. Psychiatric Res 28:295-306
76. Törk I (1990) Anatomy of the serotonergic system. Ann N Y Acad Sci 600:9-34
77. Vergnes M, Depaulis A, Boehrer A, Kempf E (1988) Selective increase of offensive behavior in the rat following intrahypothalamic 5,7-DHT-induced serotonin depletion. Behav Brain Res 29:85-91
78. Wagstaff AJ, Cheer SM, Matheson AJ, Ormrod D, Goa KL (2002) Paroxetine: an update of its use in psychiatric disorders in adults. Drugs 62:655-703
79. Walsh MT, Dinan TG (2001) Selective serotonin reuptake inhibitors and violence: a review of the available evidence. Acta Psychiatr Scand 104:84-91
80. Whishaw IQ, Kolb B (2005) The behavior of the laboratory rat: a handbook with tests. Oxford University Press, New York
81. Woolley J, Heyman I, Brammer M, Frampton I, McGuire PK, Rubia K (2008) Brain activation in paediatric obsessive compulsive disorder during tasks of inhibitory control. Br J Psychiatry 192:25-31
82. Yamamoto T, Shibata S, Ueki S (1982) Effects of locus coeruleus stimulation on muricide in olfactory bulbectomized and raphe lesioned rats. Jpn J Pharmacol 32:845-853