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Emotion processing in joint hypermobility: A potential link to the neural bases of anxiety and related somatic symptoms in collagen anomalies

Published online by Cambridge University Press:  15 April 2020

N. Mallorquí-Bagué ,
A. Bulbena ,
N. Roé-Vellvé ,
E. Hoekzema ,
S. Carmona ,
E. Barba-Müller ,
J. Fauquet ,
G. Pailhez  and
O. Vilarroya
N. Mallorquí-Bagué*
Affiliation:
Department of Psychiatry and Forensic Medicine, School of Medicine, Campus de la Universitat Autonoma de Barcelona (UAB), Barcelona, Spain Psychiatry, Psychology and Psychosomatics department, Institut Universitari Quirón Dexeus, Barcelona, Spain Neuroimaging Research Group, Fundació IMIM, Doctor Aiguader, 88, 08003Barcelona, Spain
A. Bulbena
Affiliation:
Department of Psychiatry and Forensic Medicine, School of Medicine, Campus de la Universitat Autonoma de Barcelona (UAB), Barcelona, Spain Fundació IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain Anxiety Unit, Institute of Neuropsychiatry and Addictions (INAD), Hospital del Mar, Universitat Autònoma de Barcelona, Barcelona, Spain
N. Roé-Vellvé
Affiliation:
Neuroimaging Research Group, Fundació IMIM, Doctor Aiguader, 88, 08003Barcelona, Spain
E. Hoekzema
Affiliation:
Neuroimaging Research Group, Fundació IMIM, Doctor Aiguader, 88, 08003Barcelona, Spain Netherlands Institute for Neuroscience, Meibergdreef 47, 1105 BAAmsterdam, The Netherlands
S. Carmona
Affiliation:
Neuroimaging Research Group, Fundació IMIM, Doctor Aiguader, 88, 08003Barcelona, Spain Centro de Investigación Biomédica en Red de Salud mental, Madrid, Spain Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, Spain Departamento de Bioingeniería e Ingeniería Aeroespacial, Universidad Carlos III de Madrid, Madrid, Spain
E. Barba-Müller
Affiliation:
Department of Psychiatry and Forensic Medicine, School of Medicine, Campus de la Universitat Autonoma de Barcelona (UAB), Barcelona, Spain Neuroimaging Research Group, Fundació IMIM, Doctor Aiguader, 88, 08003Barcelona, Spain
J. Fauquet
Affiliation:
Neuroimaging Research Group, Fundació IMIM, Doctor Aiguader, 88, 08003Barcelona, Spain Department Psicobiologia i Metodologia de les Ciències de la Salut, Campus de la UAB, 08193 Bellaterra (Cerdanyola del Vallés), Barcelona, Spain
G. Pailhez
Affiliation:
Department of Psychiatry and Forensic Medicine, School of Medicine, Campus de la Universitat Autonoma de Barcelona (UAB), Barcelona, Spain Fundació IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain Anxiety Unit, Institute of Neuropsychiatry and Addictions (INAD), Hospital del Mar, Universitat Autònoma de Barcelona, Barcelona, Spain
O. Vilarroya
Affiliation:
Department of Psychiatry and Forensic Medicine, School of Medicine, Campus de la Universitat Autonoma de Barcelona (UAB), Barcelona, Spain Neuroimaging Research Group, Fundació IMIM, Doctor Aiguader, 88, 08003Barcelona, Spain
*
*Corresponding author. Passeig Marítim 25, 08003 Barcelona, Spain. Tel.: +34 932483495; fax: +34 932483445. E-mail address:[email protected] (N. Mallorquí-Bagué).
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Abstract

Background:

Joint hypermobility syndrome (JHS) has repeatedly been associated with anxiety and anxiety disorders, fibromyalgia, irritable bowel syndrome and temporomandibular joint disorder. However, the neural underpinnings of these associations still remain unclear. This study explored brain responses to facial visual stimuli with emotional cues using fMRI techniques in general population with different ranges of hypermobility.

Methods:

Fifty-one non-clinical volunteers (33 women) completed state and trait anxiety questionnaire measures, were assessed with a clinical examination for hypermobility (Beighton system) and performed an emotional face processing paradigm during functional neuroimaging.

Results:

Trait anxiety scores did significantly correlate with both state anxiety and hypermobility scores. BOLD signals of the hippocampus did positively correlate with hypermobility scores for the crying faces versus neutral faces contrast in ROI analyses. No results were found for any of the other studied ROIs. Additionally, hypermobility scores were also associated with other key affective processing areas (i.e. the middle and anterior cingulate gyrus, fusiform gyrus, parahippocampal region, orbitofrontal cortex and cerebellum) in the whole brain analysis.

Conclusions:

Hypermobility scores are associated with trait anxiety and higher brain responses to emotional faces in emotion processing brain areas (including hippocampus) described to be linked to anxiety and somatic symptoms. These findings increase our understanding of emotion processing in people bearing this heritable variant of collagen and the mechanisms through which vulnerability to anxiety and somatic symptoms arises in this population.

Keywords

Functional magnetic resonance imaging (fMRI)EmotionJoint hypermobilityAnxietyPsychosomatics
Type
Original article
Information
European Psychiatry , Volume 30 , Issue 4 , June 2015 , pp. 454 - 458
Copyright
Copyright © Elsevier Masson SAS 2015

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References

Abraham, A, Kaufmann, C, Redlich, R, Hermann, A, Stark, R, Stevens, Set al.Self-referential and anxiety-relevant information processing in subclinical social anxiety: an fMRI study. Brain Imaging Behav 2013;7(1):35–48. http://dx.doi.org/10.1007/s11682-012-9188-x.CrossRefGoogle ScholarPubMed
Aoki, Y, Inokuchi, R, Suwa, HReduced N-acetylaspartate in the hippocampus in patients with fibromyalgia: a meta-analysis. Psychiatry Res 2013;30;213(3):242–248. http://dx.doi.org/10.1016/j.pscychresns.2013.03.008.CrossRefGoogle Scholar
Beighton, PHHypermobility scoring. Br J Rheumatol 1988;27:163.CrossRefGoogle ScholarPubMed
Beighton, PH, Grahame, R, Bird, HAHypermobility of joints, 2ª ed. Berlín: SpringerVerlag; 1989.CrossRefGoogle Scholar
Bianchi, S, De Lima, F, Udina, M, Martin-Santos, R, Crippa, JAAnxiety and joint hypermobility association: a systematic review. Rev Bras Psiquiatr 2012;34(Suppl. 1):S53–S68.CrossRefGoogle Scholar
Blair, RJFacial expressions, their communicatory functions and neuro-cognitive substrates. The Royal Society (Phil. Trans. R. Soc. Lond. B);2003[online].CrossRefGoogle ScholarPubMed
Brooks, SJ, Savov, V, Allzén, E, Benedict, C, Fredriksson, R, Schiöth, HBExposure to subliminal arousing stimuli induces robust activation in the amygdala, hippocampus, anterior cingulate, insular cortex and primary visual cortex: a systematic meta-analysis of fMRI studies. Neuroimage 2012;59:2962–2973. http://dx.doi.org/10.1016/j.neuroimage.2011.09.077.CrossRefGoogle ScholarPubMed
Bulbena, A, Duro, JC, Mateo, A, Porta, M, Vallejo, JJoint hypermobility syndrome and anxiety disorders. Lancet 1988;17;2(8612):694.CrossRefGoogle Scholar
Bulbena, A, Agulló, A, Pailhez, G, Martín-Santos, R, Porta, M, Guitart, Jet al.Is joint hypermobility related to anxiety in a nonclinical population also?. Psychosomatics 2004;45(5):432–437.CrossRefGoogle Scholar
Bulbena, A, Gago, J, Pailhez, G, Sperry, L, Fullana, MA, Vilarroya, OJoint hypermobility syndrome is a risk factor trait for anxiety disorders: a 15-year follow-up cohort study. Gen Hosp Psychiatry 2011;33(4):363–370.CrossRefGoogle ScholarPubMed
Eccles, JA, Beacher, FDC, Gray, MA, Jones, CL, Minati, L, Harrison, NAet al.Brain structure and joint hypermobility: relevance to the expression of psychiatric symptoms. Br J Psychiatry 2012;200:508–509.CrossRefGoogle ScholarPubMed
Endler, NS, Kocovski, NLState and trait anxiety revisited. J Anxiety Disord 2001;15(3):231–245.CrossRefGoogle Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBWEntrevista Clínica Estructurada para los Trastornos del Eje I del DSM-IV. Versión Clínica (SCID-I) Barcelona: Masson, SA; 1999.Google Scholar
Golkar, A, Lonsdorf, TB, Olsson, A, Lindstrom, KM, Berrebi, J, Fransson, Pet al.Distinct contributions of the dorsolateral prefrontal and orbitofrontal cortex during emotion regulation. PLoS One 2012;7(11):e48107. http://dx.doi.org/10.1371/journal.pone.0048107.CrossRefGoogle ScholarPubMed
Gondo, M, Moriguchi, Y, Kodama, N, Sato, N, Sudo, N, Kubo, Cet al.Daily physical complaints and hippocampal function: an fMRI study of pain modulation by anxiety. Neuroimage 2012;15;63(3):1011–1019. http://dx.doi.org/10.1016/j.neuroimage.2012.07.025.CrossRefGoogle Scholar
Grahame, RHypermobility: an important but often neglected area withinrheumatology. Nat Clin Pract Rheumatol 2008;4:522–524.CrossRefGoogle Scholar
Gur, RC, Sara, R, Hagendoorn, M, Marom, O, Hughett, P, Macy, Let al.A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. J Neurosci Methods 2002;115:137–143.CrossRefGoogle ScholarPubMed
Holzschneider, K, Mulert, CNeuroimaging in anxiety disorders. Dialogues Clin Neurosci 2011;13(4):453–461.Google ScholarPubMed
Maldjian, JA, Laurienti, PJ, Burdette, JB, Kraft, RAAn Automated Method for Neuroanatomic and Cytoarchitectonic Atlas-based Interrogation of fMRI Data Sets. Neuroimage 2003;19:1233–1239.CrossRefGoogle ScholarPubMed
Maldjian, JA, Laurienti, PJ, Burdette, JHPrecentral Gyrus Discrepancy in Electronic Versions of the Talairach Atlas. Neuroimage 2004;21(1):450–455.CrossRefGoogle ScholarPubMed
Mallorquí-Bagué, N, Garfinkel, SN, Engels, M, Eccles, JA, Pailhez, G, Bulbena, Aet al.Neuroimaging and psychophysiological investigation of the link between anxiety, enhanced affective reactivity and interoception in people with joint hypermobility. Front Psychol 2014;14(5):1162. http://dx.doi.org/10.3389/fpsyg.2014.01162.Google Scholar
Pantazatos, SP, Talati, A, Schneier, FR, Hirsch, JReduced anterior temporal and hippocampal functional connectivity during face processing discriminates individuals with social anxiety disorder from healthy controls and panic disorder, and increases following treatment. Neuropsychopharmacology 2014;39(2):425–434. http://dx.doi.org/10.1038/npp.2013.211.CrossRefGoogle ScholarPubMed
Pujol, J, Harrison, BJ, Ortiz, H, Deus, J, Soriano-Mas, C, López-Solà, Met al.Influence of the fusiform gyrus on amygdala response to emotional faces in the non-clinical range of social anxiety. Psychol Med 2009;39(7):1177–1187.CrossRefGoogle ScholarPubMed
Ross, J, Grahame, REasily missed? Joint hypermobility syndrome. Br Med J 2011;342:c7167.CrossRefGoogle Scholar
Sheehan, DV, Lecrubier, Y, Harnett-Sheehan, K, Janavs, J, Weiller, E, Bonora, LIet al.The Mini-International Neuropsychiatric Interview (MINI): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 1998;59(Suppl. 20):22–33. [In its Spanish 5.0.0 version validated in our country by Fernando L, Bobes J, Gibert J, Soto M, Soto O. Instituto IAP. 1995].Google ScholarPubMed
Smith, DM, Mizumori, SJHippocampal place cells, context, and episodic memory. Hippocampus 2006;16(9):716–729. [7].CrossRefGoogle ScholarPubMed
Smith, APR, Stephan, KE, Rugg, MD, Dolan, RJTask and content modulate amygdala-hippocampal connectivity in emotional retrieval. Neuron 2006;49(4):631–638.CrossRefGoogle ScholarPubMed
Smith, TO, Easton, V, Bacon, H, Jerman, E, Armon, K, Poland, Fet al.The relationship between benign joint hypermobility syndrome and psychological distress: a systematic review and meta-analyses. Rheumatology 2013;274–295. http://dx.doi.org/10.1093/rheumatology/ket317Google Scholar
Spielberger, CD, Gorusch, RL, Lushene, Cuestionario de Ansiedad Estado-Rasgo. Madrid: Ed: TEA; 1986.Google Scholar
Stein, JL, Wiedholz, LM, Bassett, DS, Weinberger, DR, Zink, CF, Mattay, VSet al.A validated network of effective amygdala connectivity. Neuroimage 2007;36:736–745.CrossRefGoogle ScholarPubMed
Wilken, JA, Smith, BD, Tola, K, Mann, MTrait anxiety and prior exposure to non-stressful stimuli: effects on psychophysiological arousal and anxiety. Int J Psychophysiol 2000;37(3):233–242.CrossRefGoogle ScholarPubMed
Wolf, U, Rapoport, MJ, Schweizer, TAEvaluating the affective component of the cerebellar cognitive affective syndrome. J. Neuropsychiatry Clin Neurosci 2009;21(3):245–253.CrossRefGoogle ScholarPubMed
Ziaei, M, Peira, N, Persson, JBrain systems underlying attentional control and emotional distraction during working memory encoding. Neuroimage 2014;87:276–286. http://dx.doi.org/10.1016/j.neuroimage.2013.10.048.CrossRefGoogle ScholarPubMed
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