Acute and chronic treatment with serotonin reuptake inhibitors exert opposite effects on respiration in rats: Possible implications for panic disorder

Journal of Psychopharmacology

Volumn 24, Issue 12, 2010, Pages 1793-1801

  Annerbrink, Kristina ^a   Olsson, Marie ^b   Hedner, Jan ^b   Eriksson, Elias ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

d fenfluramine; fluoxetine; m chlorophenylpiperazine; panic disorder; paroxetine; respiration; serotonin; WAY 100635

Indexed keywords

(3 CHLOROPHENYL)PIPERAZINE; 2 DIPROPYLAMINO 8 HYDROXYTETRALIN; DEXFENFLURAMINE; FLUOXETINE; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; NORFLUOXETINE; PAROXETINE; SEROTONIN;

ACUTE DRUG ADMINISTRATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREATHING; BREATHING RATE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFECT; LONG TERM CARE; MALE; NONHUMAN; PANIC; PRIORITY JOURNAL; RAT; TIDAL VOLUME;

ANIMALS; DRUG ADMINISTRATION SCHEDULE; FLUOXETINE; MALE; PANIC DISORDER; PAROXETINE; PIPERAZINES; PYRIDINES; RATS; RATS, WISTAR; RESPIRATION; SEROTONIN; SEROTONIN ANTAGONISTS; SEROTONIN UPTAKE INHIBITORS; SYNAPSES;

EID: 78650119768     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881109106908     Document Type: Article

References (73)

1. Abelson JL, Nesse RM, Weg JG, Curtis GC (1996) Respiratory psychophysiology and anxiety: cognitive intervention in the doxapram model of panic. Psychosom Med 58: 302-313.
2. Abelson JL, Weg JG, Nesse RM, Curtis GC (2001) Persistent respiratory irregularity in patients with panic disorder. Biol Psychiatry 49: 588-595.
3. Aghajanian GK, Graham AW, Sheard MH (1970) Serotonin-containing neurons in brain: depression of firing by monoamine oxidase inhibitors. Science 169: 1100-1102.
4. Annerbrink K., Olsson M., Melchior LK, Hedner J., Eriksson E. (2003) Serotonin depletion increases respiratory variability in freely moving rats: implications for panic disorder. Int J Neuropsychopharmacol 6: 51-56.
5. Arborelius L., Nomikos GG, Hertel P., et al. (1996) The 5-HT1A receptor antagonist (S)-UH-301 augments the increase in extracellular concentrations of 5-HT in the frontal cortex produced by both acute and chronic treatment with citalopram. Naunyn Schmiedebergs Arch Pharmacol 353: 630-640.
6. Bach KB, Lutcavage ME, Mitchell GS (1993) Serotonin is necessary for short-term modulation of the exercise ventilatory response. Respir Physiol 91: 57-70.
7. Battaglia M. (2002) Beyond the usual suspects: a cholinergic route for panic attacks. Mol Psychiatry 7: 239-246.
8. Battaglia M., Pesenti-Gritti P., Medland SE, Ogliari A., Tambs K., Spatola CA (2009) A genetically informed study of the association between childhood separation anxiety, sensitivity to CO(2). panic disorder, and the effect of childhood parental loss. Arch Gen Psychiatry 66: 64-71.
9. Battaglia M., Pesenti-Gritti P., Spatola CA, Ogliari A., Tambs K. (2008) A twin study of the common vulnerability between heightened sensitivity to hypercapnia and panic disorder. Am J Med Genet B Neuropsychiatr Genet 147B: 586-593.
10. Bell C., Forshall S., Adrover M., et al. (2002) Does 5-HT restrain panic? A tryptophan depletion study in panic disorder patients recovered on paroxetine. J Psychopharmacol 16: 5-14.
11. Bigos KL, Pollock BG, Aizenstein HJ, Fisher PM, Bies RR, Hariri AR (2008) Acute 5-HT reuptake blockade potentiates human amygdala reactivity. Neuropsychopharmacology 33: 3221-3225.
12. Blier P., De Montigny C. (1985) Serotoninergic but not noradrenergic neurons in rat central nervous system adapt to long-term treatment with monoamine oxidase inhibitors. Neuroscience 16: 949-955.
13. Blier P., De Montigny C. (1990) Electrophysiological investigation of the adaptive response of the 5-HT system to the administration of 5-HT1A receptor agonists. J Cardiovasc Pharmacol 15 (Suppl 7). S42-48.
14. Charney DS, Woods SW, Goodman WK, Heninger GR (1987) Serotonin function in anxiety. II. Effects of the serotonin agonist MCPP in panic disorder patients and healthy subjects. Psychopharmacology (Berl) 92: 14-24.
15. Choi H., Liao WL, Newton KM, et al. (2005) Respiratory abnormalities resulting from midcervical spinal cord injury and their reversal by serotonin 1A agonists in conscious rats. J Neurosci 25: 4550-4559.
16. Den Boer JA, Westenberg HG (1988) Effect of a serotonin and noradrenaline uptake inhibitor in panic disorder; a double-blind comparative study with fluvoxamine and maprotiline. Int Clin Psychopharmacol 3: 59-74.
17. Edwards E., Whitaker-Azmitia PM, Harkins K. (1990) 5-HT1A and 5-HT1B agonists play a differential role on the respiratory frequency in rats. Neuropsychopharmacology 3: 129-136.
18. Eriksson E., Engberg G., Bing O., Nissbrandt H. (1999) Effects of mCPP on the extracellular concentrations of serotonin and dopamine in rat brain. Neuropsychopharmacology 20: 287-296.
19. Feldman JL, Mitchell GS, Nattie EE (2003) Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 26: 239-266.
20. Fornal CA, Metzler CW, Gallegos RA, Veasey SC, Mccreary AC, Jacobs BL (1996) WAY-100635, a potent and selective 5-hydroxytryptamine1A antagonist, increases serotonergic neuronal activity in behaving cats: comparison with (S)-WAY-100135. J Pharmacol Exp Ther 278: 752-762.
21. Forster EA, Cliffe IA, Bill DJ, et al. (1995) A pharmacological profile of the selective silent 5-HT1A receptor antagonist, WAY-100635. Eur J Pharmacol 281: 81-88.
22. Garattini S., Mennini T., Samanin R. (1987) From fenfluramine racemate to d-fenfluramine. Specificity and potency of the effects on the serotoninergic system and food intake. Ann N Y Acad Sci 499: 156-166.
23. Gorman JM, Askanazi J., Liebowitz MR, et al. (1984) Response to hyperventilation in a group of patients with panic disorder. Am J Psychiatry 141: 857-861.
24. Gorman JM, Fyer MR, Goetz R., et al. (1988) Ventilatory physiology of patients with panic disorder. Arch Gen Psychiatry 45: 31-9.
25. Harmer CJ, Mackay CE, Reid CB, Cowen PJ, Goodwin GM (2006) Antidepressant drug treatment modifies the neural processing of nonconscious threat cues. Biol Psychiatry 59: 816-820.
26. Henderson DR, Konkle DM, Mitchell GS (1999) Effects of serotonin re-uptake inhibition on ventilatory control in goats. Respir Physiol 115: 1-10.
27. Hjorth S. (1993) Serotonin 5-HT1A autoreceptor blockade potentiates the ability of the 5-HT reuptake inhibitor citalopram to increase nerve terminal output of 5-HT in vivo: a microdialysis study. J Neurochem 60: 776-779.
28. Invernizzi R., Bramante M., Samanin R. (1996) Role of 5-HT1A receptors in the effects of acute chronic fluoxetine on extracellular serotonin in the frontal cortex. Pharmacol Biochem Behav 54: 143-147.
29. Johnson PL, Hollis JH, Moratalla R., Lightman SL, Lowry CA (2005) Acute hypercarbic gas exposure reveals functionally distinct subpopulations of serotonergic neurons in rats. J Psychopharmacol 19: 327-341.
30. Kasamo K., Suzuki T., Tada K., et al. (2001) Endogenous 5-HT tonically inhibits spontaneous firing activity of dorsal hippocampus CA1 pyramidal neurons through stimulation of 5-HT(1A) receptors in quiet awake rats: in vivo electrophysiological evidence. Neuropsychopharmacology 24: 141-151.
31. Kent JM, Papp LA, Martinez JM, et al. (2001) Specificity of panic response to CO(2) inhalation in panic disorder: a comparison with major depression and premenstrual dysphoric disorder. Am J Psychiatry 158: 58-67.
32. Klein DF (1993) False suffocation alarms, spontaneous panics, and related conditions. An integrative hypothesis. Arch Gen Psychiatry 50: 306-317.
33. Laferrere B., Wurtman RJ (1989) Effect of D-fenfluramine on serotonin release in brains of anaesthetized rats. Brain Res 504: 258-263.
34. Lee YJ, Curtis GC, Weg JG, Abelson JL, Modell JG, Campbell KM (1993) Panic attacks induced by doxapram. Biol Psychiatry 33: 295-297.
35. Liebowitz MR, Fyer AJ, Gorman JM, et al. (1984) Lactate provocation of panic attacks. I. Clinical and behavioral findings. Arch Gen Psychiatry 41: 764-770.
36. Manzke T., Guenther U., Ponimaskin EG, et al. (2003) 5-HT4(a) receptors avert opioid-induced breathing depression without loss of analgesia. Science 301: 226-229.
37. Martin-Body RL, Grundy HR (1985) Effects of neurotoxin-induced brainstem lesions on the respiratory responses of conscious rats. Clin Exp Pharmacol Physiol 12: 427-437.
38. Martinez JM, Kent JM, Coplan JD, et al. (2001) Respiratory variability in panic disorder. Depress Anxiety 14: 232-237.
39. Mendelson WB, Martin JV, Rapoport DM (1990) Effects of buspirone on sleep and respiration. Am Rev Respir Dis 141: 1527-1530.
40. Mitchell GS, Smith CA, Vidruk H., Jameson LC, Dempsey JA (1983) Effects of p-chlorophenylalanine on ventilatory control in goats. J Appl Physiol 54: 277-283.
41. Mlinar B., Tatini F., Ballini C., Nencioni S., Della Corte L., Corradetti R. (2005) Differential autoinhibition of 5-hydroxytryptamine neurons by 5-hydroxytryptamine in the dorsal raphe nucleus. Neuroreport 16: 1351-1355.
42. Modigh K., Westber P., Eriksson E. (1992) Superiority of clomipramine over imipramine in the treatment of panic disorder: a placebo-controlled trial. J Clin Psychopharmacol 12: 251-261.
43. Mortimore C., Anderson IM (2000) d-Fenfluramine in panic disorder: a dual role for 5-hydroxytryptamine. Psychopharmacology (Berl) 149: 251-258.
44. Mulkey DK, Stornetta RL, Weston MC, et al. (2004) Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 7: 1360-1369.
45. Nardi AE, Freire RC, Zin WA (2008 a) Panic disorder and control of breathing. Respir Physiol Neurobiol.
46. Nardi AE, Freire RC, Zin WA (2009) Panic disorder and control of breathing. Respir Physiol Neurobiol 167 (1). 133-143.
47. Nardi AE, Valenca AM, Nascimento I., et al. (2008 b) A caffeine challenge test in panic disorder patients, their healthy first-degree relatives, and healthy controls. Depress Anxiety 25: 847-853.
48. Nutt DJ, Glue P. (1989) Clinical pharmacology of anxiolytics and antidepressants: a psychopharmacological perspective. Pharmacol Ther 44: 309-334.
49. Olson EB, Jr (1987) Ventilatory adaptation to hypoxia occurs in serotonin-depleted rats. Respir Physiol 69: 227-235.
50. Olsson M., Annerbrink K., Bengtsson F., Hedner J., Eriksson E. (2004) Paroxetine influences respiration in rats: implications for the treatment of panic disorder. Eur Neuropsychopharmacol 14: 29-37.
51. Papp LA, Klein DF, Gorman JM (1993) Carbon dioxide hypersensitivity, hyperventilation, and panic disorder. Am J Psychiatry 150: 1149-1157.
52. Papp LA, Martinez JM, Klein DF, et al. (1997) Respiratory psychophysiology of panic disorder: three respiratory challenges in 98 subjects. Am J Psychiatry 154: 1557-1565.
53. Perna G., Battaglia M., Garberi A., Arancio C., Bertani A., Bellodi L. (1994) Carbon dioxide/oxygen challenge test in panic disorder. Psychiatry Res 52: 159-171.
54. Pitts FN, Jr, McClure JN, Jr (1967) Lactate metabolism in anxiety neurosis. N Engl J Med 277: 1329-1336.
55. Pohl R., Yeragani VK, Balon R., Lycaki H. (1988) The jitteriness syndrome in panic disorder patients treated with antidepressants. J Clin Psychiatry 49: 100-104.
56. Preter M., Klein DF (2008) Panic, suffocation false alarms, separation anxiety and endogenous opioids. Prog Neuropsychopharmacol Biol Psychiatry 32: 603-612.
57. Richerson GB (2004) Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 5: 449-461.
58. Richerson GB, Wang W., Hodges MR, Dohle CI, Diez-Sampedro A. (2005) Homing in on the specific phenotype(s) of central respiratory chemoreceptors. Exp Physiol 90: 259-266 ; discussion 266-269.
59. Richter DW, Manzke T., Wilken B., Ponimaskin E. (2003) Serotonin receptors: guardians of stable breathing. Trends Mol Med 9: 542-548.
60. Severson CA, Wang W., Pieribone VA, Dohle CI, Richerson GB (2003) Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci 6: 1139-1140.
61. Sharp T., Bramwell SR, Grahame-Smith DG (1989) 5-HT1 agonists reduce 5-hydroxytryptamine release in rat hippocampus in vivo as determined by brain microdialysis. Br J Pharmacol 96: 283-290. (Pubitemid 19045101)
62. Sheehan DV, Raj AB, Harnett-Sheehan K., Soto S., Knapp E. (1993) The relative efficacy of high-dose buspirone and alprazolam in the treatment of panic disorder: a double-blind placebo-controlled study. Acta Psychiatr Scand 88: 1-11.
63. Sinha S., Papp LA, Gorman JM (2000) How study of respiratory physiology aided our understanding of abnormal brain function in panic disorder. J Affect Disord 61: 191-200.
64. Stahl SM (1998) Mechanism of action of serotonin selective reuptake inhibitors. Serotonin receptors and pathways mediate therapeutic effects and side effects. J Affect Disord 51: 215-235.
65. Stein MB, Millar TW, Larsen DK, Kryger H. (1995) Irregular breathing during sleep in patients with panic disorder. Am J Psychiatry 152: 1168-1173.
66. Stone RA, Worsdell YM, Fuller RW, Barnes PJ (1993) Effects of 5-hydroxytryptamine and 5-hydroxytryptophan infusion on the human cough reflex. J Appl Physiol 74: 396-401.
67. Struzik L., Duffin J., Vermani M., Hegadoren K., Katzman MA (2002) Effects of tryptophan depletion on central and peripheral chemoreflexes in man. Respir Physiol Neurobiol 133: 183-195.
68. Taylor NC, Li A., Green A., Kinney HC, Nattie EE (2004) Chronic fluoxetine microdialysis into the medullary raphe nuclei of the rat, but not systemic administration, increases the ventilatory response to CO2. J Appl Physiol 97: 1763-1773.
69. Toru I., Shlik J., Maron E., Vasar V., Nutt DJ (2006) Tryptophan depletion does not modify response to CCK-4 challenge in patients with panic disorder after treatment with citalopram. Psychopharmacology (Berl) 186: 107-112.
70. Valic M., Pecotic R., Dogas Z. (2008) Phrenic nerve activity is enhanced by 5-HT1A receptor agonist 8-OH-DPAT in spontaneously breathing anesthetized rats. J Physiol Pharmacol 59: 17-25.
71. Van Vliet IM, Westenberg HG, Den Boer JA (1996) Effects of the 5-HT1A receptor agonist flesinoxan in panic disorder. Psychopharmacology (Berl) 127: 174-180.
72. Wang X., Dergacheva O., Kamendi H., Gorini C., Mendelowitz D. (2007) 5-Hydroxytryptamine 1A/7 and 4alpha receptors differentially prevent opioid-induced inhibition of brain stem cardiorespiratory function. Hypertension 50: 368-376.
73. Wilhelm FH, Trabert W., Roth WT (2001) Physiologic instability in panic disorder and generalized anxiety disorder. Biol Psychiatry 49: 596-605.