Serotonin 2A receptors, citalopram and tryptophan-depletion: A multimodal imaging study of their interactions during response inhibition

Neuropsychopharmacology

Volumn 38, Issue 6, 2013, Pages 996-1005

  Macoveanu, Julian ^a,b   Hornboll, Bettina ^a,b   Elliott, Rebecca ^c   Erritzoe, David ^b,d   Paulson, Olaf B ^a,b,d   Siebner, Hartwig ^a,b   Knudsen, Gitte M ^b,d   Rowe, James B ^b,e  

^a Mental Health Services CPH   (Denmark)

^b Center for Integrated Molecular Brain Imaging   (Denmark)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

5 HT2A receptor; altanserin; citalopram; fMRI; inhibition; serotonin

Indexed keywords

ALTANSERIN; CITALOPRAM; FLUORINE 18; SEROTONIN 2A RECEPTOR; TRYPTOPHAN;

ADULT; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMPULSIVENESS; INFERIOR FRONTAL GYRUS; MALE; NORMAL HUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN DEPLETION; RECEPTOR BINDING; SEROTONIN BLOOD LEVEL;

ADULT; BRAIN; CITALOPRAM; COHORT STUDIES; FEMALE; HUMANS; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; PHOTIC STIMULATION; POSITRON-EMISSION TOMOGRAPHY; PSYCHOMOTOR PERFORMANCE; REACTION TIME; RECEPTOR, SEROTONIN, 5-HT2A; TRYPTOPHAN; YOUNG ADULT;

EID: 84878592634     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.264     Document Type: Article

References (63)

1. Adams KH, Hansen ES, Pinborg LH, Hasselbalch SG, Svarer C, Holm S et al (2005). Patients with obsessive-compulsive disorder have increased 5-HT2A receptor binding in the caudate nuclei. Int J Neuropsychopharmacol 8: 391-401.
2. Adams KH, Pinborg LH, Svarer C, Hasselbalch SG, Holm S, Haugbol S et al (2004). A database of [(18)F]-altanserin binding to 5-HT(2A) receptors in normal volunteers: normative data and relationship to physiological and demographic variables. Neuroimage 21: 1105-1113.
3. Anderson IM, Clark L, Elliott R, Kulkarni B, Williams SR, Deakin JF (2002). 5-HT(2C) receptor activation by m-chlorophenylpiperazine detected in humans with fMRI. Neuroreport 13: 1547-1551.
4. Ardis TC, Cahir M, Elliott JJ, Bell R, Reynolds GP, Cooper SJ (2009). Effect of acute tryptophan depletion on noradrenaline and dopamine in the rat brain. J Psychopharmacol 23: 51-55.
5. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6: 115-116.
6. Asahi S, Okamoto Y, Okada G, Yamawaki S, Yokota N (2004). Negative correlation between right prefrontal activity during response inhibition and impulsiveness: a fMRI study. Eur Arch Psychiatry Clin Neurosci 254: 245-251.
7. Attenburrow MJ, Mitter PR, Whale R, Terao T, Cowen PJ (2001). Low-dose citalopram as a 5-HT neuroendocrine probe. Psychopharmacology (Berl) 155: 323-326.
8. Blokland A, Lieben C, Deutz NE (2002). Anxiogenic and depressive-like effects, but no cognitive deficits, after repeated moderate tryptophan depletion in the rat. J Psychopharmacol 16: 39-49.
9. Chamberlain SR, Hampshire A, Muller U, Rubia K, Del Campo N, Craig K et al (2009). Atomoxetine modulates right inferior frontal activation during inhibitory control: a pharmacological functional magnetic resonance imaging study. Biol Psychiatry 65: 550-555.
10. Chikazoe J, Jimura K, Asari T, Yamashita K, Morimoto H, Hirose S et al (2009). Functional dissociation in right inferior frontal cortex during performance of go/no-go task. Cereb Cortex 19: 146-152.
11. Chikazoe J, Konishi S, Asari T, Jimura K, Miyashita Y (2007). Activation of right inferior frontal gyrus during response inhibition across response modalities. J Cogn Neurosci 19: 69-80.
12. Clarke HF, Dalley JW, Crofts HS, Robbins TW, Roberts AC (2004). Cognitive inflexibility after prefrontal serotonin depletion. Science 304: 878-880.
13. Del-Ben CM, Deakin JF, McKie S, Delvai NA, Williams SR, Elliott R et al (2005). The effect of citalopram pretreatment on neuronal responses to neuropsychological tasks in normal volunteers: an FMRI study. Neuropsychopharmacology 30: 1724-1734.
14. Dodds CM, Morein-Zamir S, Robbins TW (2011). Dissociating inhibition, attention, and response control in the frontoparietal network using functional magnetic resonance imaging. Cereb Cortex 21: 1155-1165.
15. Eagle DM, Bari A, Robbins TW (2008). The neuropsychopharmacology of action inhibition: cross-species translation of the stop-signal and go/no-go tasks. Psychopharmacology (Berl) 199: 439-456.
16. Erritzoe D, Holst K, Frokjaer VG, Licht CL, Kalbitzer J, Nielsen FA et al (2010). A nonlinear relationship between cerebral serotonin transporter and 5-HT(2A) receptor binding: an in vivo molecular imaging study in humans. J Neurosci 30: 3391-3397.
17. Evers EA, van der Veen FM, van Deursen JA, Schmitt JA, Deutz NE, Jolles J (2006). The effect of acute tryptophan depletion on the BOLD response during performance monitoring and response inhibition in healthy male volunteers. Psychopharmacology (Berl) 187: 200-208.
18. Frokjaer VG, Mortensen EL, Nielsen FA, Haugbol S, Pinborg LH, Adams KH et al (2008). Frontolimbic serotonin 2A receptor binding in healthy subjects is associated with personality risk factors for affective disorder. Biol Psychiatry 63: 569-576.
19. Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM (2010). The role of the right inferior frontal gyrus: inhibition and attentional control. Neuroimage 50: 1313-1319.
20. Hannon J, Hoyer D (2008). Molecular biology of 5-HT receptors. Behav Brain Res 195: 198-213.
21. Harrison AA, Everitt BJ, Robbins TW (1999). Central serotonin depletion impairs both the acquisition and performance of a symmetrically reinforced go/no-go conditional visual discrimination. Behav Brain Res 100: 99-112.
22. Haugbol S, Pinborg LH, Regeur L, Hansen ES, Bolwig TG, Nielsen FA et al (2007). Cerebral 5-HT2A receptor binding is increased in patients with Tourette's syndrome. Int J Neuropsychopharmacol 10: 245-252.
23. Henning J, Netter P (2002). Oral application of citalopram (20 mg) and its usefulness for neuroendocrine challenge tests. Int J Neuropsychopharmacol 5: 67-71.
24. Henson R (2006). Forward inference using functional neuroimaging: dissociations versus associations. Trends Cogn Sci 10: 64-69.
25. Huey ED, Putnam KT, Grafman J (2006). A systematic review of neurotransmitter deficits and treatments in frontotemporal dementia. Neurology 66: 17-22.
26. Iversen SD, Mishkin M (1970). Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity. Exp Brain Res 11: 376-386.
27. Kenner NM, Mumford JA, Hommer RE, Skup M, Leibenluft E, Poldrack RA (2010). Inhibitory motor control in response stopping and response switching. J Neurosci 30: 8512-8518.
28. Konishi S, Nakajima K, Uchida I, Kikyo H, Kameyama M, Miyashita Y (1999). Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 122: 981-991.
29. Konishi S, Nakajima K, Uchida I, Sekihara K, Miyashita Y (1998). No-go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging. Eur J Neurosci 10: 1209-1213.
30. Lamar M, Cutter WJ, Rubia K, Brammer M, Daly EM, Craig MC et al (2009). 5-HT, prefrontal function and aging: fMRI of inhibition and acute tryptophan depletion. Neurobiol Aging 30: 1135-1146.
31. Lancaster J, Woldorff M, Parsons L, Liotti M, Freitas C, Rainey L et al (2000). Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10: 120-131.
32. Langenecker SA, Kennedy SE, Guidotti LM, Briceno EM, Own LS, Hooven T et al (2007). Frontal and limbic activation during inhibitory control predicts treatment response in major depressive disorder. Biol Psychiatry 62: 1272-1280.
33. LeMarquand DG, Pihl RO, Young SN, Tremblay RE, Seguin JR, Palmour RM et al (1998). Tryptophan depletion, executive functions, and disinhibition in aggressive, adolescent males. Neuropsychopharmacology 19: 333-341.
34. Levy BJ, Wagner AD (2011). Cognitive control and right ventrolateral prefrontal cortex: reflexive reorienting, motor inhibition, and action updating. Ann N Y Acad Sci 1224: 40-62.
35. Leyton M, Okazawa H, Diksic M, Paris J, Rosa P, Mzengeza S et al (2001). Brain regional alpha-[11C]methyl-L-tryptophan trapping in impulsive subjects with borderline personality disorder. Am J Psychiatry 158: 775-782.
36. Logan GD, Cowan WB, Davis KA (1984). On the ability to inhibit simple and choice reaction time responses: a model and a method. J Exp Psychol Hum Percept Perform 10: 276-291.
37. Lund TE, Norgaard MD, Rostrup E, Rowe JB, Paulson OB (2005). Motion or activity: their role in intra-and inter-subject variation in fMRI. Neuroimage 26: 960-964.
38. Marner L, Knudsen GM, Haugbol S, Holm S, Baare W, Hasselbalch SG (2009). Longitudinal assessment of cerebral 5-HT2A receptors in healthy elderly volunteers: an (18F)-altanserin PET study. Eur J Nucl Med Mol Imaging 36: 287-293.
39. Masaki D, Yokoyama C, Kinoshita S, Tsuchida H, Nakatomi Y, Yoshimoto K et al (2006). Relationship between limbic and cortical 5-HT neurotransmission and acquisition and reversal learning in a go/no-go task in rats. Psychopharmacology (Berl) 189: 249-258.
40. McKie S, Del-Ben C, Elliott R, Williams S, del Vai N, Anderson I et al (2005). Neuronal effects of acute citalopram detected by pharmacoMRI. Psychopharmacology (Berl) 180: 680-686.
41. McNair D, Lorr M, Droppleman L (1971). Manual for the Profile of Mood States. Educational and Industrial Testing Services: San Diego, CA.
42. Moret C, Briley M (1996). Effects of acute and repeated administration of citalopram on extracellular levels of serotonin in rat brain. Eur J Pharmacol 295: 189-197.
43. Mostofsky SH, Simmonds DJ (2008). Response inhibition and response selection: two sides of the same coin. J Cogn Neurosci 20: 751-761.
44. Nomura M, Nomura Y (2006). Psychological, neuroimaging, and biochemical studies on functional association between impulsive behavior and the 5-HT2A receptor gene polymorphism in humans. Ann N Y Acad Sci 1086: 134-143.
45. Pinborg LH, Adams KH, Svarer C, Holm S, Hasselbalch SG, Haugbol S et al (2003). Quantification of 5-HT2A receptors in the human brain using [18F]altanserin-PET and the bolus/infusion approach. J Cereb Blood Flow Metab 23: 985-996.
46. Pinborg LH, Adams KH, Yndgaard S, Hasselbalch SG, Holm S, Kristiansen H et al (2004). (18F)altanserin binding to human 5HT2A receptors is unaltered after citalopram and pindolol challenge. J Cereb Blood Flow Metab 24: 1037-1045.
47. Pinborg LH, Arfan H, Haugbol S, Kyvik KO, Hjelmborg JV, Svarer C et al (2008). The 5-HT2A receptor binding pattern in the human brain is strongly genetically determined. Neuroimage 40: 1175-1180.
48. Ridderinkhof KR, van den Wildenberg WP, Segalowitz SJ, Carter CS (2004). Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn 56: 129-140.
49. Rowe J, Friston K, Frackowiak R, Passingham R (2002). Attention to action: specific modulation of corticocortical interactions in humans. Neuroimage 17: 988-998.
50. Rubia K, Lee F, Cleare AJ, Tunstall N, Fu CH, Brammer M et al (2005). Tryptophan depletion reduces right inferior prefrontal activation during response inhibition in fast, event-related fMRI. Psychopharmacology (Berl) 179: 791-803.
51. Rubia K, Russell T, Overmeyer S, Brammer MJ, Bullmore ET, Sharma T et al (2001). Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage 13: 250-261.
52. Ruhe HG, Mason NS, Schene AH (2007). Mood is indirectly related to serotonin, norepinephrine and dopamine levels in humans: a meta-analysis of monoamine depletion studies. Mol Psychiatry 12: 331-359.
53. Simmonds DJ, Pekar JJ, Mostofsky SH (2008). Meta-analysis of Go/ No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 46: 224-232.
54. Svarer C, Madsen K, Hasselbalch SG, Pinborg LH, Haugbol S, Frokjaer VG et al (2005). MR-based automatic delineation of volumes of interest in human brain PET images using probability maps. Neuroimage 24: 969-979.
55. Swann N, Tandon N, Canolty R, Ellmore TM, McEvoy LK, Dreyer S et al (2009). Intracranial EEG reveals a time-and frequencyspecific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J Neurosci 29: 12675-12685.
56. Swick D, Ashley V, Turken AU (2008). Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci 9: 102.
57. van Donkelaar EL, Blokland A, Ferrington L, Kelly PA, Steinbusch HW, Prickaerts J (2011). Mechanism of acute tryptophan depletion: is it only serotonin? Mol Psychiatry 16: 695-713.
58. Wager TD, Sylvester CY, Lacey SC, Nee DE, Franklin M, Jonides J (2005). Common and unique components of response inhibition revealed by fMRI. Neuroimage 27: 323-340.
59. Walderhaug E, Lunde H, Nordvik JE, Landro NI, Refsum H, Magnusson A (2002). Lowering of serotonin by rapid tryptophan depletion increases impulsiveness in normal individuals. Psychopharmacology (Berl) 164: 385-391.
60. Williams WA, Shoaf SE, Hommer D, Rawlings R, Linnoila M (1999). Effects of acute tryptophan depletion on plasma and cerebrospinal fluid tryptophan and 5-hydroxyindoleacetic acid in normal volunteers. J Neurochem 72: 1641-1647.
61. Wingrove J, Bond AJ, Cleare AJ, Sherwood R (1999). Trait hostility and prolactin response to tryptophan enhancement/depletion. Neuropsychobiology 40: 202-206.
62. Zepf FD, Holtmann M, Stadler C, Demisch L, Schmitt M, Wockel L et al (2008). Diminished serotonergic functioning in hostile children with ADHD: tryptophan depletion increases behavioural inhibition. Pharmacopsychiatry 41: 60-65.
63. Zheng D, Oka T, Bokura H, Yamaguchi S (2008). The key locus of common response inhibition network for no-go and stop signals. J Cogn Neurosci 20: 1434-1442.