Expression and co-expression of serotonin and dopamine transporters in social anxiety disorder: a multitracer positron emission tomography study.


Journal

Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835

Informations de publication

Date de publication:
08 2021
Historique:
received: 04 03 2019
accepted: 21 11 2019
revised: 20 11 2019
pubmed: 12 12 2019
medline: 28 1 2022
entrez: 12 12 2019
Statut: ppublish

Résumé

Serotonin and dopamine are putatively involved in the etiology and treatment of anxiety disorders, but positron emission tomography (PET) studies probing the two neurotransmitters in the same individuals are lacking. The aim of this multitracer PET study was to evaluate the regional expression and co-expression of the transporter proteins for serotonin (SERT) and dopamine (DAT) in patients with social anxiety disorder (SAD). Voxel-wise binding potentials (BP

Identifiants

pubmed: 31822819
doi: 10.1038/s41380-019-0618-7
pii: 10.1038/s41380-019-0618-7
doi:

Substances chimiques

Dopamine Plasma Membrane Transport Proteins 0
Serotonin Plasma Membrane Transport Proteins 0
Serotonin 333DO1RDJY
Dopamine VTD58H1Z2X

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3970-3979

Informations de copyright

© 2019. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Stein MB, Stein DJ. Social anxiety disorder. Lancet 2008;371:1115–25.
pubmed: 18374843
Brühl AB, Delsignore A, Komossa K, Weidt S. Neuroimaging in social anxiety disorder—a meta-analytic review resulting in a new neurofunctional model. Neurosci Biobehav Rev. 2014;47:260–80.
pubmed: 25124509
Berger M, Gray JA, Roth BL. The expanded biology of serotonin. Annu Rev Med. 2009;60:355–66.
pubmed: 19630576 pmcid: 5864293
Gordon JA, Hen R. The serotonergic system and anxiety. Neuromolecular Med 2004;5:27–40.
pubmed: 15001810
Mayo-Wilson E, Dias S, Mavranezouli I, Kew KMA, Clark DM, Ades A, et al. Psychological and pharmacological interventions for social anxiety disorder in adults: a systematic review and network meta-analysis. Lancet Psychiatry 2014;1:368–76.
pubmed: 26361000 pmcid: 4287862
Lanzenberger RR, Mitterhauser M, Spindelegger C, Wadsak W, Klein N, Mien LK, et al. Reduced serotonin-1A receptor binding in social anxiety disorder. Biol Psychiatry. 2007;61:1091–89.
Frick A, Åhs F, Engman J, Jonasson M, Alaie I, Björkstrand J. et al. Serotonin synthesis and reuptake in social anxiety disorder a positron emission tomography study. JAMA Psychiatry. 2015;72:794–802.
pubmed: 26083190
Furmark T, Marteinsdottir I, Frick A, Heurling K, Tillfors M, Appel L, et al. Serotonin synthesis rate and the tryptophan hydroxylase-2: G-703T polymorphism in social anxiety disorder. J Psychopharmacol 2016;30:1028–35.
pubmed: 27189957
Frick A, Åhs F, Appel L, Jonasson M, Wahlstedt K, Bani M, et al. Reduced serotonin synthesis and regional cerebral blood flow after anxiolytic treatment of social anxiety disorder. Eur Neuropsychopharmacol 2016;26:1775–83.
pubmed: 27642077
van der Wee NJ, van Veen JF, Stevens H, van Vliet IM, van Rijk PP, Westenberg HG. Increased serotonin and dopamine transporter binding in psychotropic medication-naive patients with generalized social anxiety disorder shown by 123I-beta-(4-iodophenyl)-tropane SPECT. J Nucl Med. 2008;49:757–63.
pubmed: 18413401
Houle S, Ginovart N, Hussey D, Meyer JH, Wilson AA. Imaging the serotonin transporter with positron emission tomography: initial human studies with [11C]DAPP and [11C]DASB. Eur J Nucl Med. 2000;27:1719–22.
pubmed: 11105830
Lammel S, Ion DI, Roeper J, Malenka RC. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron. 2011;70:855–62.
pubmed: 21658580 pmcid: 3112473
de Jong JW, Afjei SA, Pollak Dorocic I, Peck JR, Liu C, Kim C, et al. A neural circuit mechanism for encoding aversive stimuli in the mesolimbic dopamine system. Neuron. 2019;101:133–51.
pubmed: 30503173
Smillie LD, Wacker J. Dopaminergic foundations of personality and individual differences. Front Hum Neurosci 2014;8:874.
pubmed: 25400570 pmcid: 4214189
Berridge KC, Kringelbach ML. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology. 2008;199:457–80.
pubmed: 18311558 pmcid: 3004012
Wacker J, Smillie LD. Trait extraversion and dopamine function. Soc Personal Psychol Compass 2015;9:225–38.
Berridge KC, Kringelbach ML. Pleasure systems in the brain. Neuron. 2015;86:646–64.
pubmed: 25950633 pmcid: 4425246
Richey JA, Ghane M, Valdespino A, Coffman MC, Strege MV, White SW, et al. Spatiotemporal dissociation of brain activity underlying threat and reward in social anxiety disorder. Soc Cogn Affect Neurosci. 2017;12:81–94.
Doruyter A, Dupont P, Stein DJ, Lochner C, Warwick JM. Nuclear neuroimaging in social anxiety disorder: a review. J Nucl Med. 2018;59:1794–800.
pubmed: 30291197
Schneier FR, Liebowitz MR, Abi-dargham A, Zea-ponce Y, Lin S-H, Laruelle M. Low dopamine D 2 receptor binding potential in social phobia. Am J Psychiatry. 2000;157:457–9.
pubmed: 10698826
Schneier FR, Martinez D, Abi-Dargham A, Zea-Ponce Yolanda, Simpson HB, Liebowitz MR, et al. Striatal dopamine D2 receptor availability in OCD with and without comorbid social anxiety disorder: preliminary findings. Depress Anxiety. 2008;25:1–7.
pubmed: 17252580
Schneier FR, Abi-dargham A, Martinez D, Slifstein M, Whang DR, Liebowitz MR, et al. Dopamine transporters, D2 receptors, and dopamine release in generalized social anxiety disorder. Depress Anxiety. 2009;8:1–8.
Plavén-Sigray P, Hedman E, Victorsson P, Matheson GJ, Forsberg A, Djurfeldt DR, et al. Extrastriatal dopamine D2-receptor availability in social anxiety disorder. Eur Neuropsychopharmacol. 2017;27:462–9.
pubmed: 28377075
Tiihonen J, Kuikka J, Bergström K, Lepola U, Koponen H, Leinonen E. Dopamine reuptake site densities in patients with social phobia. Am J Psychiatry. 1997;154:239–42.
pubmed: 9016274
Warwick JM, Carey PD, Cassimjee N, Lochner S, Hemmings H, Smook-Moolman H, et al. Dopamine transporter binding in social anxiety disorder: the effect of treatment with escitalopram. Metab Brain Dis. 2012;27:151–8.
pubmed: 22350963
Appel L, Jonasson M, Danfors T, Nyholm D, Askmark H, Lubberink M, et al. Use of 11C-PE2I PET in differential diagnosis of parkinsonian disorders. J Nucl Med. 2015;56:234–42.
pubmed: 25593112
Gray JA, McNaughton N. The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. New York: Oxford University Press; 2000.
Cloninger RC. A unified diosocial theory of personality and its role in the development of anxiety states. Psychiatr Dev. 1986;4:167–226.
pubmed: 3809156
Kimbrel NA. A model of the development and maintenance of generalized social phobia. Clin Psychol Rev. 2008;28:592–612.
pubmed: 17959288
Corr PJ, McNaughton N. Neuroscience and approach/avoidance personality traits: A two stage (valuation-motivation) approach. Neurosci Biobehav Rev. 2012;36:2339–54.
pubmed: 23041073
Dewey SL, Smith GS, Logan J, Alexoff D, Ding YS, King P, et al. Serotonergic modulation of striatal dopamine measured with positron emission tomography (PET) and in viva microdialysis. J Neurosci. 1995;75:921–9.
Smith GS, Ma Y, Dhawan V, Chaly T, Eidelberg D. Selective serotonin reuptake inhibitor (SSRI) modulation of striatal dopamine measured with [11C]-raclopride and positron emission tomography. Synapse. 2009;63:1–6.
pubmed: 18925655 pmcid: 4617661
Daws LC. Unfaithful neurotransmitter transporters: focus on serotonin uptake and implications for antidepressant efficacy. Pharm Ther. 2009;121:89–99.
Nakamura K. The role of the dorsal raphé nucleus in reward-seeking behavior. Front Integr Neurosci. 2013;7:1–18.
Esposito E, Di Matteo V, Di Giovanni G. Serotonin-dopamine interaction: an overview. Prog Brain Res. 2008;172:3–6.
pubmed: 18772025
Dray A, Gonye TJ, Oakley NR, Tanner T. Evidence for the existence of a raphe projection to the substantia nigra in rat. Brain Res. 1976;113:45–57.
pubmed: 953733
Forstner AJ, Rambau S, Friedrich N, Ludwig KU, Böhmer AC, Mangold E, et al. Further evidence for genetic variation at the serotonin transporter gene SLC6A4 contributing toward anxiety. Psychiatr Genet. 2017;27:96–102.
pubmed: 28272115
Rhodes RA, Murthy NV, Dresner MA, Selvaraj S, Stavrakakis N, Babar S, et al. Human 5-HT transporter availability predicts amygdala reactivity in vivo. J Neurosci. 2007;27:9233–7.
pubmed: 17715358 pmcid: 6672189
Furmark T, Tillfors M, Garpenstrand H, Marteinsdottir I, Långström B, Oreland L, et al. Serotonin transporter polymorphism related to amygdala excitability and symptom severity in patients with social phobia. Neurosci Lett. 2004;362:189–92.
pubmed: 15158011
Furmark T, Henningsson S, Appel L, Åhs F, Linnman C, Pissiota A, et al. Genotype over diagnosis in amygdala responsiveness: affective processing in social anxiety disorder. J Psychiatry Neurosci. 2009;34:30–40.
pubmed: 19125211 pmcid: 2612081
Bergman O, Åhs F, Furmark T, Appel L, Linnman C, Faria V, et al. Association between amygdala reactivity and a dopamine transporter gene polymorphism. Transl Psychiatry 2014;4:e420.
pubmed: 25093598 pmcid: 4150236
American Psychiatric Association. Diagnostic and statistical manual of mental disorders. Text Revision (DSM-IV-TR). 4th ed. Arlington: American Psychiatric Association; 2000.
Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, et al. The mini-international neuropsychiatric interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 1998;59:22–33.
pubmed: 9881538
Rytwinski NK, Fresco DM, Heimberg RG, Coles ME, Liebowitz LR, Cissel S, et al. Screening for social anxiety disorder with the self-report version of the Liebowitz Social Anxiety Scale. Depress Anxiety. 2009;26:34–8.
pubmed: 18781659
Logan J, Fowler JS, Volkow ND, Wang G-J, Ding Y-S, Alexoff DL. Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab. 1996;16:834–40.
pubmed: 8784228
Gunn RN, Lammertsma AA, Hume SP, Cunningham VJ. Parametric imaging of ligand-receptor binding in PET using a simplified reference region model. Neuroimage. 1997;6:279–87.
pubmed: 9417971
Jonasson M, Appel L, Engman J, Frick A, Nyholm D, Askmark H, et al. Validation of parametric methods for [
pubmed: 23435214
Svarer C, Madsen K, Hasselbalch SG, Pinborg LH, Haugbøl S, Frøkjær VG, et al. MR-based automatic delineation of volumes of interest in human brain PET images using probability maps. Neuroimage. 2005;24:969–79.
pubmed: 15670674
Frick A, Åhs F, Palmquist ÅM, Pissiota A, Wallenquist U, Fernandez M, et al. Overlapping expression of serotonin transporters and neurokinin-1 receptors in posttraumatic stress disorder: a multi-tracer PET study. Mol Psychiatry. 2016;21:1400–7.
pubmed: 26619809
Plavén-Sigray P, Gustavsson P, Farde L, Borg J, Stenkrona P, Nyberg L, et al. Dopamine D1 receptor availability is related to social behavior: a positron emission tomography study. Neuroimage. 2014;102:590–5.
pubmed: 25134976
Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19:1233–9.
pubmed: 12880848
Hammers A, Allom R, Koepp MJ, Free SL, Myers R, Lemieux L, et al. Three-dimensional maximum probability atlas of the human brain, with particular reference to the temporal lobe. Hum Brain Mapp. 2003;19:224–47.
pubmed: 12874777 pmcid: 6871794
Öhman A. The role of the amygdala in human fear: automatic detection of threat. Psychoneuroendocrinology. 2005;30:953–8.
pubmed: 15963650
Adhikari A, Lerner TN, Finkelstein J, Pak S, Jennings JH, Davidson TJ, et al. Basomedial amygdala mediates top-down control of anxiety and fear. Nature. 2015;527:179–85.
pubmed: 26536109 pmcid: 4780260
Hensler JG. Serotonergic modulation of the limbic system. Neurosci Biobehav Rev. 2006;30:203–14.
pubmed: 16157378
Salgado-Pineda P, Delaveau P, Blin O, Nieoullon A. Dopaminergic contribution to the regulation of emotional perception. Clin Neuropharmacol. 1979;28:228–37.
Schultz W. Reward functions of the basal ganglia. J Neural Transm. 2016;123:679–93.
pubmed: 26838982
Bas-Hoogendam JM, van Steenbergen H, Pannekoek NJ, Fouche JP, Lochner C, Hattingh CJ, et al. Voxel-based morphometry multi-center mega-analysis of brain structure in social anxiety disorder. NeuroImage Clin. 2017;16:678–88.
pubmed: 30140607 pmcid: 6103329
Carlezon WA, Thomas MJ. Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology. 2009;56:122–32.
pubmed: 18675281
Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN. Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron. 2008;59:1037–50.
pubmed: 18817740 pmcid: 2742320
Cardinal RN, Parkinson JA, Hall J, Everitt BJ. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev. 2002;26:321–52.
pubmed: 12034134
Moran RJ, Kishida KT, Lohrenz T, Saez I, Laxton AW, Witcher MR, et al. The protective action encoding of serotonin transients in the human brain. Neuropsychopharmacology. 2018;43:1425–35.
pubmed: 29297512 pmcid: 5916372
Browne CJ, Abela AR, Chu D, Li Z, Ji X, Lambe EK, et al. Dorsal raphe serotonin neurons inhibit operant responding for reward via inputs to the ventral tegmental area but not the nucleus accumbens: evidence from studies combining optogenetic stimulation and serotonin reuptake inhibition. Neuropsychopharmacology. 2018;44:793–804.
pubmed: 30420603 pmcid: 6372654
Shirayama Y, Chaki S. Neurochemistry of the nucleus accumbens and its relevance to depression and antidepressant action in rodents. Curr Neuropharmacol. 2006;4:277–91.
pubmed: 18654637 pmcid: 2475798
Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE, Cho S, et al. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature. 2011;475:377–80.
pubmed: 21716290 pmcid: 3775282
Oler JA, Fox AS, Shelton SE, Christian BT, Dhanabalan M, Oakes TR, et al. Serotonin transporter availability in the amygdala and bed nucleus of the stria terminalis predicts anxious temperament and brain glucose metabolic activity. J Neurosci. 2009;29:9961–6.
pubmed: 19675230 pmcid: 2756094
Takano A, Arakawa R, Hayashi M, Takahashi H, Ito H, Suhara T. Relationship between neuroticism personality trait and serotonin transporter binding. Biol Psychiatry. 2007;62:588–92.
pubmed: 17336939
Moriyama TS, Felicio AC, Chagas MHN, Tardelli VS, Ferraz HB, Tumas V, et al. Increased dopamine transporter density in Parkinson’s disease patients with social anxiety disorder. J Neurol Sci. 2011;310:53–7.
pubmed: 21783205
Fisher PM, Meltzer CC, Ziolko SK, Price JC, Hariri AR. Capacity for 5-HT1A-mediated autoregulation predicts amygdala reactivity. Nat Neurosci. 2006;9:1362–3.
pubmed: 17013380
Näslund J, Studer E, Pettersson R, Hagsäter M, Nilsson S, Nissbrandt H, et al. Differences in anxiety-like behaviour within a batch of Wistar rats are associated with differences in serotonergic transmission, enhanced by acute SSRI administration and abolished by serotonin depletion. Int J Neuropsychopharmacol. 2015;18:pyv018.
pubmed: 25716782 pmcid: 4571633
Sossi V, De La Fuente-Fernández R, Schulzer M, Troiano AR, Ruth TJ, Stoessl AJ. Dopamine transporter relation to dopamine turnover in Parkinson’s disease: a positron emission tomography study. Ann Neurol. 2007;62:468–74.
pubmed: 17886297
Zhuang X, Oosting RS, Jones SR, Gainetdinov RR, Miller GW, Caron MG, et al. Hyperactivity and impaired response habituation in hyperdopaminergic mice. Proc Natl Acad Sci. 2001;98:1982–87.
pubmed: 11172062 pmcid: 29368
Carpenter AC, Saborido TP, Stanwood GD. Development of hyperactivity and anxiety responses in dopamine transporter-deficient mice. Dev Neurosci 2012;34:250–7.
pubmed: 22572477
Richey JA, Rittenberg A, Hughes L, Damiano CR, Sabatino A, Miller S, et al. Common and distinct neural features of social and non-social reward processing in autism and social anxiety disorder. Soc Cogn Affect Neurosci. 2014;9:367–77.
pubmed: 23223206
Farde L, Plavén-Sigray P, Borg J, Cervenka S. Brain neuroreceptor density and personality traits: towards dimensional biomarkers for psychiatric disorders. Philos Trans R Soc B Biol Sci. 2018;373:20170156.

Auteurs

Olof R Hjorth (OR)

Department of Psychology, Uppsala University, Uppsala, Sweden. olof.hjorth@psyk.uu.se.

Andreas Frick (A)

Department of Psychology, Uppsala University, Uppsala, Sweden.
The Beijer Laboratory, Department of Neuroscience, Psychiatry, Uppsala University, Uppsala, Sweden.
Department of Neuroscience, Psychiatry, Uppsala University, Uppsala, Sweden.

Malin Gingnell (M)

Department of Psychology, Uppsala University, Uppsala, Sweden.
Department of Neuroscience, Psychiatry, Uppsala University, Uppsala, Sweden.

Johanna M Hoppe (JM)

Department of Psychology, Uppsala University, Uppsala, Sweden.

Vanda Faria (V)

Department of Psychology, Uppsala University, Uppsala, Sweden.
Center for Pain and the Brain, Department of Anesthesiology Perioperative and Pain Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA.
Smell & Taste Clinic, Department of Otorhinolaryngology, TU Dresden, Dresden, Germany.

Sara Hultberg (S)

Department of Psychology, Uppsala University, Uppsala, Sweden.

Iman Alaie (I)

Department of Neuroscience, Child and Adolescent Psychiatry, Uppsala University, Uppsala, Sweden.

Kristoffer N T Månsson (KNT)

Centre for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany.
Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.
Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Berlin, Germany.

Kurt Wahlstedt (K)

Department of Psychology, Uppsala University, Uppsala, Sweden.

My Jonasson (M)

Department of Surgical Sciences-Nuclear medicine and PET, Uppsala University, Uppsala, Sweden.

Mark Lubberink (M)

Department of Surgical Sciences-Nuclear medicine and PET, Uppsala University, Uppsala, Sweden.

Gunnar Antoni (G)

Department of Medicinal Chemistry, Uppsala University, Uppsala, Sweden.

Mats Fredrikson (M)

Department of Psychology, Uppsala University, Uppsala, Sweden.
Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.

Tomas Furmark (T)

Department of Psychology, Uppsala University, Uppsala, Sweden.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH