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Disrupted Functional Connectivity of the Pain Network in Fibromyalgia

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Disrupted Functional Connectivity of the Pain Network in Fibromyalgia Published Ahead of Print on December 30, 2011 as 10.1097/PSY.0b013e3182408f04 Disrupted Functional Connectivity of the Pain Network in Fibromyalgia IGNACIO CIFRE,PHD, CAROLINA SITGES,PHD, DANIEL FRAIMAN,PHD, MIGUEL A´ NGEL MUN˜ OZ,PHD, PABLO BALENZUELA,PHD, ANA GONZA´ LEZ-ROLDA´ N, MS, MERCEDES MARTI´NEZ-JAUAND, MS, NIELS BIRBAUMER,PHD, DANTE R. CHIALVO,MD, AND PEDRO MONTOYA,PHD Objective: To investigate the impact of chronic pain on brain dynamics at rest. Methods: Functional connectivity was examined in patients with fibromyalgia (FM) (n = 9) and healthy controls (n = 11) by calculating partial correlations between low-frequency blood oxygen levelYdependent fluctuations extracted from 15 brain regions. Results: Patients with FM had more positive and negative correlations within the pain network than healthy controls. Patients with FM displayed enhanced functional connectivity of the anterior cingulate cortex (ACC) with the insula (INS) and basal ganglia ( p values between .01 and .05), the secondary somatosensory area with the caudate (CAU) (p = .012), the primary motor cortex with the supplementary motor area (p = .007), the globus pallidus with the amygdala and superior temporal sulcus (both p values G .05), and the medial prefrontal cortex with the posterior cingulate cortex (PCC) and CAU (both p values G .05). Functional connectivity of the ACC with the amygdala and periaqueductal gray (PAG) matter (p values between .001 and .05), the thalamus with the INS and PAG (both p values G .01), the INS with the putamen (p = .038), the PAG with the CAU (p = .038), the secondary somatosensory area with the motor cortex and PCC (both p values G .05), and the PCC with the superior temporal sulcus (p = .002) was also reduced in FM. In addition, significant negative correlations were observed between depression and PAG connectivity strength with the thalamus (r = j0.64, p = .003) and ACC (r = j0.60, p = .004). Conclusions: These findings demonstrate that patients with FM display a substantial imbalance of the connectivity within the pain network during rest, suggest- ing that chronic pain may also lead to changes in brain activity during internally generated thought processes such as occur at rest. Key words: fibromyalgia, chronic pain, resting state, functional connectivity, partial correlation analysis. BOLD = blood oxygen levelYdependent; FM = fibromyalgia; HC = somatosensory cortices (SII), and thalamus (THA), which com- healthy control; WHYMPI = West Haven-Yale Multidimensional prise the so-called pain network (2). This functional network Pain Inventory; fMRI = functional magnetic resonance imaging; has been viewed as a dynamic neural substrate of the subjec- ACC = anterior cingulate cortex; PCC = posterior cingulate cortex; tive experience of pain modulated by sensory, cognitive, and AMYG = amygdala; CAU = caudate; PUT = putamen; INS = affective factors. Little is known, however, about the dynamic insula; M1 = primary motor area; SMA = supplementary motor area; properties of this pain network and its intrinsic functional SI = primary somatosensory area; SII = secondary somatosensory area; mPFC = medial prefrontal cortex; PAG = periaqueductal gray; connectivity during spontaneous pain as compared with STS = superior temporal sulcus; THA = thalamus. chronic pain (3). The study of spontaneous blood oxygen levelYdependent (BOLD) activity when subjects are asked to rest quietly in the INTRODUCTION scanner has provided insight into the functional topography of he understanding of brain correlates involved in pain pro- the brain and the coherence patterns of functionally intercon- Tcessing has increased significantly since the advent of neu- nected networks not related to specific tasks (4). In this sense, roimaging techniques (1). Most studies have revealed that the recent work has shown that spatial cross-correlations and the processing of painful stimuli is associated with the increased estimation of independent components in low-frequency spon- activation of several brain regions, such as the insular cortex, taneous fluctuations (G0.1 Hz) of BOLD time series acquired anterior cingulate cortex (ACC), primary (SI) and secondary under resting-state conditions are useful tools to analyze spatial patterns of coherent brain activity within different functional networks involved in somatosensory, motor, visual, auditory, or From the Research Institute on Health Sciences (I.C., C.S., M.A´ .M., A.G.-R., executive functions (5). Moreover, enhanced functional con- M.M.-J., P.M.), University of Balearic Islands, Palma, Spain; Consejo Nacional de Investigaciones Cientı´ficas y Tecnolo´gicas (D.F., P.B., D.R.C.); Departamento nectivity strength measured by positive or negative correlations de Ciencias (D.F.), Universidad de San Andres; Departamento de Fı´sica (P.B.), across spontaneous BOLD fluctuations has been associated with Universidad de Buenos Aires, Buenos Aires, Argentina; Institute of Medical increases in neuronal synchrony or asynchrony (6), respec- Psychology and Behavioral Neurobiology (N.B.), University of Tu¨bingen, Tu¨bingen, Germany; Ospedale San Camillo (N.B.), Instituto di Ricovero e Cura a tively, suggesting that regions with similar functionality tend to Carattere Scientifico, Venezia, Italy; and Department of Physiology (D.R.C.), be positively correlated in their spontaneous BOLD activity, David Geffen School of Medicine, University of California, Los Angeles, whereas regions with apparently opposing functionality are neg- California. Address correspondence and reprint requests to Pedro Montoya, PhD, Research atively correlated or anticorrelated. Analyses of resting-state Institute on Health Sciences, University of the Balearic Islands, Cra. Valldemossa functional connectivity have also been applied in neuropsy- km 7.5, 07122 Palma de Mallorca, Spain. E-mail: [email protected] chiatric disorders such as major depression (7) or chronic pain This work was supported by the Spanish Ministry of Science and Innovation Y (Plan Nacional de I+D+I and European Regional Development Funds; grant (8 10), showing that persistent, emotionally laden, self-reflective numbers SEJ2007-62312 and JCI-2008-03074); National Institute of Neuro- tendencies in depressed subjects are linked to increased func- logical Disorder and Stroke, National Institutes of Health (grant number tional connectivity in the medial prefrontal cortex (mPFC) and NS58661 to Dr. Chialvo); Consejo Nacional de Investigaciones Cientı´ficas y Tecnolo´gicas (Argentina); Deutsche Forschungsgemeinschaft; German Federal that persistent pain is associated with greater connectivity of the Ministry of Education and Research; and the Bernstein Center for Computa- insula (INS). Because these two brain regions are also relevant tional Neuroscience (Germany). parts of the pain network and given the strong relationships No conflicts of interest were declared by any of the authors. Received for publication March 24, 2011; revision received September 5, 2011. between depression and chronic pain, it seems plausible that DOI: 10.1097/PSY.0b013e3182408f04 spontaneous and persistent pain as it occurs in chronic pain states Psychosomatic Medicine 74:00Y00 (2012) 1 0033-3174/12/7401Y0000 Copyright * 2012 by the American Psychosomatic Society Copyright © 2011 by the American Psychosomatic Society. Unauthorized reproduction of this article is prohibited. I. CIFRE et al. could be affecting the brain dynamics of the pain network. TABLE 1. Data Obtained From Patients’ and Healthy Nevertheless, to our knowledge, there is no information about Controls’ Questionnaires the intrinsic functional connectivity of all brain regions within HC (n = 11) FM (n =9) t the pain network in patients with chronic pain. In the present study, we examined low-frequency fluctua- Age, y j0.688 tions of resting-state BOLD signals in fibromyalgia (FM), a M (SD) 49.0 (12.1) 52.3 (8.9) functional somatic syndrome characterized by widespread pain Range 23Y61 33Y65 sensations and affective symptoms (11). Although the under- Sex lying etiology of FM still remains unclear, altered activations of Male 2 1 several brain regions in the pain network (thalamic nuclei, so- Female 9 8 matosensory cortices, ACC, INS, and prefrontal cortices) have Pain beginning, V 25.6 (16.6) already been reported during the sensory processing of acute M (SD), y pain (12Y15). Moreover, it has been suggested that abnormal Pain duration, V 26.8 (17.4) pain processing in FM might be modulated by the patient’s M (SD), y mood and the affective context in which body sensations are Medication V felt (16). On the basis of previous findings, we hypothesize that Antidepressants 8 V functional connectivity within the pain network should be al- Analgesics/relaxants/ 4 NSAIDs tered in FM even when patients are experiencing spontaneous Anxiolytics V 8 fluctuations of their pain at rest. We assumed that the intrinsic BDI score j4.992* functional connectivity of brain regions within the pain network M (SD) 8.1 (6.3) 29.78 (12.07) would be greater and much more extended in patients with FM Range 3Y21 2Y44 than in controls, reflecting the diffuse and complex patterns of WHYMPI, M (SD) symptoms in these patients. In particular, we expected that (range = 0Y6) brain regions involved in the processing of affective (i.e., ACC Social support V 4.0 (1.4) (1.5Y6.0) and INS) and sensory pain components (i.e., somatosensory Affective distress V 4.1 (1.0) (2.3Y5.5) cortex and THA) would show enhanced connectivity to other Pain interference V 4.0 (1.7) (1.3Y5.7) brain regions of the pain network in FM, whereas brain regions Pain intensity V 4.5 (0.9) (3.3Y5.5) involved in pain modulation, such as the periaqueductal gray Life control V 2.8 (0.5) (2.0Y3.5) (PAG) matter, would display reduced connectivity. Distracting responses V 4.1 (1.6) (1.0Y6.0) Solicitous responses V 3.1 (1.6) (0.2Y4.8) Punishing responses V 1.5 (1.4) (0.0Y3.7) Household chores V 3.2 (1.3) (1.2Y5.2) MATERIALS AND METHODS Activities away V 1.7 (1.3) (0.0Y3.8) Participants from home The study was conducted at the Research Center for Neurological Dis- Outdoor work V 0.9 (0.6) (0.0Y2.0) eases (Madrid, Spain) between March 2009 and July 2009.
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