Attenuation of fear-like response by escitalopram treatment after electrical stimulation of the midbrain dorsolateral periaqueductal gray

Experimental Neurology

Volumn 226, Issue 2, 2010, Pages 293-300

  Lim, Lee Wei ^a,b,c,d   Blokland, Arjan ^c,d   Tan, Sonny ^a,b,c,d   Vlamings, Rinske ^a,b,c,d   Sesia, Thibaut ^e   Aziz Mohammadi, Mujzgan ^a,b,c,d   Visser Vandewalle, Veerle ^b,c   Steinbusch, Harry W M ^a,d   Schruers, Koen ^c,d   Temel, Yasin ^a,b,c,d  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d European Graduate School of Neuroscience   (Netherlands)

^e UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Agoraphobia; Anticipatory anxiety; Electrical stimulation; Panic disorder; Periaqueductal gray

Indexed keywords

BUSPIRONE; ESCITALOPRAM;

ACUTE DRUG ADMINISTRATION; AGORAPHOBIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN DEPTH STIMULATION; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED RESPONSE; FEAR; MALE; NONHUMAN; OPEN FIELD TEST; PANIC; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; SINGLE DRUG DOSE;

ANIMALS; ANTI-ANXIETY AGENTS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; BUSPIRONE; CITALOPRAM; DEEP BRAIN STIMULATION; ESCAPE REACTION; EXPLORATORY BEHAVIOR; FEAR; LOCOMOTION; MALE; PERIAQUEDUCTAL GRAY; RATS; RATS, WISTAR;

EID: 77958493029     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.08.035     Document Type: Article

References (69)

1. Abbar M. Panic disorder and panic attack. Encephale 1996, 22(Spec No 5):13-18.
2. Amano K., Tanikawa T., Iseki H., Kawabatake H., Notani M., Kawamura H., Kitamura K. Single neuron analysis of the human midbrain tegmentum. Rostral mecencephalic reticulotomy for pain relief. Appl. Neurophysiol. 1978, 41:66-78.
3. Practice guideline for the treatment of patients with panic disorder. Work Group on Panic Disorder. Am. J. Psychiatry 1998, 155(5 Suppl):1-34. American-Psychiatric-Association, (May).
4. Diagnostic and Statistical Manual of Mental Disorders 2000, American-Psychiatric-Association, American Psychiatric Press, Washington, DC, Text Revision. Fourth ed.
5. Argyropoulos S.V., Hood S.D., Adrover M., Bell C.J., Rich A.S., Nash J.R., Rich N.C., Witchel H.J., Nutt D.J. Tryptophan depletion reverses the therapeutic effect of selective serotonin reuptake inhibitors in social anxiety disorder. Biol. Psychiatry 2004, 56:503-509.
6. Assie M.B., Lomenech H., Ravailhe V., Faucillon V., Newman-Tancredi A. Rapid desensitization of somatodendritic 5-HT1A receptors by chronic administration of the high-efficacy 5-HT1A agonist, F13714: a microdialysis study in the rat. Br. J. Pharmacol. 2006, 149:170-178.
7. Beitz A.J., Clements J.R., Mullett M.A., Ecklund L.J. Differential origin of brainstem serotoninergic projections to the midbrain periaqueductal gray and superior colliculus of the rat. J. Comp. Neurol. 1986, 250:498-509.
8. Bondi C.O., Rodriguez G., Gould G.G., Frazer A., Morilak D.A. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 2008, 33:320-331.
9. Borelli K.G., Nobre M.J., Brandao M.L., Coimbra N.C. Effects of acute and chronic fluoxetine and diazepam on freezing behavior induced by electrical stimulation of dorsolateral and lateral columns of the periaqueductal gray matter. Pharmacol. Biochem. Behav. 2004, 77:557-566.
10. Bouton M.E., Mineka S., Barlow D.H. A modern learning theory perspective on the etiology of panic disorder. Psychol. Rev. 2001, 108:4-32.
11. Brandao M.L., Lopez-Garcia J.A., Graeff F.G., Roberts M.H. Electrophysiological evidence for excitatory 5-HT2 and depressant 5-HT1A receptors on neurones of the rat midbrain tectum. Brain Res. 1991, 556:259-266.
12. Broiz A.C., Oliveira L.C., Brandao M.L. Regulation of conditioned and unconditioned fear in rats by 5-HT1A receptors in the dorsal periaqueductal gray. Pharmacol. Biochem. Behav. 2008, 89:76-84.
13. Burghardt N.S., Sullivan G.M., McEwen B.S., Gorman J.M., LeDoux J.E. The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biol. Psychiatry 2004, 55:1171-1178.
14. Cassano G.B., Savino M. Symptomatology of panic disorder: an attempt to define the panic-agoraphobic spectrum phenomenology. Psychopharmacology of Panic 1993, 38-57. Oxford University Press, New York. S.A. Montgomery (Ed.).
15. Ceglia I., Acconcia S., Fracasso C., Colovic M., Caccia S., Invernizzi R.W. Effects of chronic treatment with escitalopram or citalopram on extracellular 5-HT in the prefrontal cortex of rats: role of 5-HT1A receptors. Br. J. Pharmacol. 2004, 142:469-478.
16. Connor K.M., Davidson J.R. Generalized anxiety disorder: neurobiological and pharmacotherapeutic perspectives. Biol. Psychiatry 1998, 44:1286-1294.
17. Dawson L.A., Nguyen H.Q., Smith D.I., Schechter L.E. Effects of chronic fluoxetine treatment in the presence and absence of (+/-)pindolol: a microdialysis study. Br. J. Pharmacol. 2000, 130:797-804.
18. de Bortoli V.C., Nogueira R.L., Zangrossi H. Effects of fluoxetine and buspirone on the panicolytic-like response induced by the activation of 5-HT1A and 5-HT2A receptors in the rat dorsal periaqueductal gray. Psychopharmacology (Berl.) 2006, 183:422-428.
19. De Vry J. 5-HT1A receptor agonists: recent developments and controversial issues. Psychopharmacology (Berl.) 1995, 121:1-26.
20. 2. J. Psychopharmacol. 2009, 23:975-978.
21. Graeff F.G. Serotonin, the periaqueductal gray and panic. Neurosci. Biobehav. Rev. 2004, 28:239-259.
22. Graeff F.G., Del-Ben C.M. Neurobiology of panic disorder: from animal models to brain neuroimaging. Neurosci. Biobehav. Rev. 2008, 32:1326-1335.
23. Griez E., Schruers K. Experimental pathophysiology of panic. J. Psychosom. Res. 1998, 45:493-503.
24. Griez E.J.L., Faravelli C., Nutt D., Zohar J. Anxiety Disorders: an Introduction to Clinical Management and Research 2001.
25. Hamon M., Gozlan H., el Mestikawy S., Emerit M.B., Bolanos F., Schechter L. The central 5-HT1A receptors: pharmacological, biochemical, functional, and regulatory properties. Ann. N. Y. Acad. Sci. 1990, 600:114-129. (discussion 129-131).
26. Hashimoto S., Inoue T., Koyama T. Serotonin reuptake inhibitors reduce conditioned fear stress-induced freezing behavior in rats. Psychopharmacology (Berl.) 1996, 123:182-186.
27. Hogg S., Michan L., Jessa M. Prediction of anti-panic properties of escitalopram in the dorsal periaqueductal grey model of panic anxiety. Neuropharmacology 2006, 51:141-145.
28. Hollander E., Simeon D. Anxiety disorders. Textbook of Clinical Psychiatry 2003, 543-565. American Psychiatric Publishing, Washington, DC. 4th ed.
29. Inoue T., Hashimoto S., Tsuchiya K., Izumi T., Ohmori T., Koyama T. Effect of citalopram, a selective serotonin reuptake inhibitor, on the acquisition of conditioned freezing. Eur. J. Pharmacol. 1996, 311:1-6.
30. Inoue T., Tsuchiya K., Koyama T. Serotonergic activation reduces defensive freezing in the conditioned fear paradigm. Pharmacol. Biochem. Behav. 1996, 53:825-831.
31. Invernizzi R., Bramante M., Samanin R. Chronic treatment with citalopram facilitates the effect of a challenge dose on cortical serotonin output: role of presynaptic 5-HT1A receptors. Eur. J. Pharmacol. 1994, 260:243-246.
32. Jenck F., Broekkamp C.L., Van Delft A.M. The effect of antidepressants on aversive periaqueductal gray stimulation in rats. Eur. J. Pharmacol. 1990, 177:201-204.
33. Jenck F., Moreau J.L., Martin J.R. Dorsal periaqueductal gray-induced aversion as a simulation of panic anxiety: elements of face and predictive validity. Psychiatry Res. 1995, 57:181-191.
34. Jenck F., Moreau J.L., Berendsen H.H., Boes M., Broekkamp C.L., Martin J.R., Wichmann J., Van Delft A.M. Antiaversive effects of 5HT2C receptor agonists and fluoxetine in a model of panic-like anxiety in rats. Eur. Neuropsychopharmacol. 1998, 8:161-168.
35. Kakui N., Yokoyama F., Yamauchi M., Kitamura K., Imanishi T., Inoue T., Koyama T. Anxiolytic-like profile of mirtazapine in rat conditioned fear stress model: functional significance of 5-hydroxytryptamine 1A receptor and alpha1-adrenergic receptor. Pharmacol. Biochem. Behav. 2009, 92:393-398.
36. Klerman G.L., Weissman M.M., Ouellette R., Johnson J., Greenwald S. Panic attacks in the community. Social morbidity and health care utilization. JAMA 1991, 265:742-746.
37. Liebowitz M.R., Fyer A.J., Gorman J.M., Dillon D., Appleby I.L., Levy G., Anderson S., Levitt M., Palij M., Davies S.O., et al. Lactate provocation of panic attacks. I. Clinical and behavioral findings. Arch. Gen. Psychiatry 1984, 41:764-770.
38. Liebowitz M.R., Gorman J.M., Fyer A.J., Levitt M., Dillon D., Levy G., Appleby I.L., Anderson S., Palij M., Davies S.O., et al. Lactate provocation of panic attacks. II. Biochemical and physiological findings. Arch. Gen. Psychiatry 1985, 42:709-719.
39. Lim L.W., Blokland A., Visser-Vandewalle V., Vlamings R., Sesia T., Steinbusch H., Schruers K., Griez E., Temel Y. High-frequency stimulation of the dorsolateral periaqueductal gray and ventromedial hypothalamus fails to inhibit panic-like behaviour. Behav. Brain Res. 2008, 193:197-203.
40. Lim L.W., Temel Y., Sesia T., Vlamings R., Visser-Vandewalle V., Steinbusch H.W., Blokland A. Buspirone induced acute and chronic changes of neural activation in the periaqueductal gray of rats. Neuroscience 2008, 155:164-173.
41. Lim L.W., Temel Y., Visser-Vandewalle V., Steinbusch H., Schruers K., Hameleers R., Esquivel G., Griez E., Blokland A. Effect of buspirone on the behavioral regulation of rats in low versus high anxiety conditions. Arzneimittelforschung 2008, 58:269-276.
42. Lim L.W., Temel Y., Visser-Vandewalle V., Blokland A., Steinbusch H. Fos immunoreactivity in the rat forebrain induced by electrical stimulation of the dorsolateral periaqueductal gray matter. J. Chem. Neuroanat. 2009, 38:83-96.
43. Lovick T.A., Parry D.M., Stezhka V.V., Lumb B.M. Serotonergic transmission in the periaqueductal gray matter in relation to aversive behaviour: morphological evidence for direct modulatory effects on identified output neurons. Neuroscience 2000, 95:763-772.
44. Lugenbiel P., Sartorius A., Vollmayr B., Schloss P. Creatine transporter expression after antidepressant therapy in rats bred for learned helplessness. World J. Biol. Psychiatry 2009, 1-5.
45. Nashold B.S., Wilson W.P., Slaughter D.G. Sensations evoked by stimulation in the midbrain of man. J. Neurosurg. 1969, 30:14-24.
46. Ninan P.M.S. Buspirone and gepirone. Textbook of Psychopharmcology 2004, 391-404. American Psychiatric Publishing, Washington, DC. 3rd ed. A.F. Schatzberg, C.B. Nemeroff (Eds.).
47. Nogueira R.L., Graeff F.G. Role of 5-HT receptor subtypes in the modulation of dorsal periaqueductal gray generated aversion. Pharmacol. Biochem. Behav. 1995, 52:1-6.
48. Oliveira L.C., Broiz A.C., de Macedo C.E., Landeira-Fernandez J., Brandao M.L. 5-HT2 receptor mechanisms of the dorsal periaqueductal gray in the conditioned and unconditioned fear in rats. Psychopharmacology (Berl.) 2007, 191:253-262.
49. Overbeek T., Schruers K., van Leeuwen I.D., Klaassen T., Griez E. Experimental affective symptoms in panic disorder patients. Can. J. Psychiatry 2005, 50:175-178.
50. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press. 4th ed.
51. Pobbe R.L., Zangrossi H. 5-HT(1A) and 5-HT(2A) receptors in the rat dorsal periaqueductal gray mediate the antipanic-like effect induced by the stimulation of serotonergic neurons in the dorsal raphe nucleus. Psychopharmacology (Berl.) 2005, 183:314-321.
52. Poltronieri S.C., Zangrossi H., de Barros Viana M. Antipanic-like effect of serotonin reuptake inhibitors in the elevated T-maze. Behav. Brain Res. 2003, 147:185-192.
53. Quartermain D., Clemente J., Shemer A. 5-HT1A agonists disrupt memory of fear conditioning in mice. Biol. Psychiatry 1993, 33:247-254.
54. Roy-Byrne P.P., Craske M.G., Stein M.B. Panic disorder. Lancet 2006, 368:1023-1032.
55. Sanchez C., Bergqvist P.B., Brennum L.T., Gupta S., Hogg S., Larsen A., Wiborg O. Escitalopram, the S-(+)-enantiomer of citalopram, is a selective serotonin reuptake inhibitor with potent effects in animal models predictive of antidepressant and anxiolytic activities. Psychopharmacology (Berl.) 2003, 167:353-362.
56. Sato H., Skelin I., Debonnel G., Diksic M. Chronic buspirone treatment normalizes open field behavior in olfactory bulbectomized rats: assessment with a quantitative autoradiographic evaluation of the 5-HT1A binding sites. Brain Res. Bull. 2008, 75:545-555.
57. Schenberg L.C., Bittencourt A.S., Sudre E.C., Vargas L.C. Modeling panic attacks. Neurosci. Biobehav. Rev. 2001, 25:647-659.
58. Schenberg L.C., Capucho L.B., Vatanabe R.O., Vargas L.C. Acute effects of clomipramine and fluoxetine on dorsal periaqueductal grey-evoked unconditioned defensive behaviours of the rat. Psychopharmacology (Berl.) 2002, 159:138-144.
59. 2 provoked panic in panic disorder. J. Psychopharmacol. 2004, 18:553-558.
60. Schruers K., Klaassen T., Pols H., Overbeek T., Deutz N.E., Griez E. Effects of tryptophan depletion on carbon dioxide provoked panic in panic disorder patients. Psychiatry Res. 2000, 93:179-187.
61. Schruers K., van Diest R., Overbeek T., Griez E. Acute L-5-hydroxytryptophan administration inhibits carbon dioxide-induced panic in panic disorder patients. Psychiatry Res. 2002, 113:237-243.
62. Schutz M.T., de Aguiar J.C., Graeff F.G. Anti-aversive role of serotonin in the dorsal periaqueductal grey matter. Psychopharmacology (Berl.) 1985, 85:340-345.
63. Temel Y., Visser-Vandewalle V., van der Wolf M., Spincemaille G.H., Desbonnet L., Hoogland G., Steinbusch H.W. Monopolar versus bipolar high frequency stimulation in the rat subthalamic nucleus: differences in histological damage. Neurosci. Lett. 2004, 367:92-96.
64. Temel Y., Boothman L.J., Blokland A., Magill P.J., Steinbusch H.W., Visser-Vandewalle V., Sharp T. Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17087-17092.
65. Tunnicliff G., Brokaw J.J., Hausz J.A., Matheson G.K., White G.W. Influence of repeated treatment with buspirone on central 5-hydroxytryptamine and dopamine synthesis. Neuropharmacology 1992, 31:991-995.
66. Vargas L.C., Schenberg L.C. Long-term effects of clomipramine and fluoxetine on dorsal periaqueductal grey-evoked innate defensive behaviours of the rat. Psychopharmacology (Berl.) 2001, 155:260-268.
67. Vianna D.M., Landeira-Fernandez J., Brandao M.L. Dorsolateral and ventral regions of the periaqueductal gray matter are involved in distinct types of fear. Neurosci. Biobehav. Rev. 2001, 25:711-719.
68. Wittchen H.U. Natural course and spontaneous remissions of untreated anxiety disorders-results of the Munich follow-up study (MFS). Panic and Phobias: 2. Treatments and Variables Affecting Course and Outcome 1988, 3-17. Springer, Berlin. I. Hand, H.U. Wittchen (Eds.).
69. Zanoveli J.M., Nogueira R.L., Zangrossi H. Chronic imipramine treatment sensitizes 5-HT1A and 5-HT 2 A receptors in the dorsal periaqueductal gray matter: evidence from the elevated T-maze test of anxiety. Behav. Pharmacol. 2005, 16:543-552.