Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-31T15:57:46.963Z Has data issue: false hasContentIssue false
  • English
  • Français

Corticostriatal functional connectivity in non-medicated patients with obsessive-compulsive disorder

Published online by Cambridge University Press:  16 April 2020

Y. Sakai ,
J. Narumoto ,
S. Nishida ,
T. Nakamae ,
K. Yamada ,
T. Nishimura  and
K. Fukui
Y. Sakai*
Affiliation:
Department of Psychiatry, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto 602-8566, Japan
J. Narumoto
Affiliation:
Department of Psychiatry, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto 602-8566, Japan
S. Nishida
Affiliation:
Department of Psychiatry, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto 602-8566, Japan
T. Nakamae
Affiliation:
Department of Psychiatry, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto 602-8566, Japan
K. Yamada
Affiliation:
Department of Radiology, Graduate School of Medical Science Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto 602-8566, Japan
T. Nishimura
Affiliation:
Department of Radiology, Graduate School of Medical Science Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto 602-8566, Japan
K. Fukui
Affiliation:
Department of Psychiatry, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto 602-8566, Japan
*
*Corresponding author. Tel.: +81 75 251 5612, fax: +81 75 251 5839. E-mail address: [email protected] (Y. Sakai).
Get access

Abstract

The basal ganglia represents a key component of the pathophysiological model for obsessive-compulsive disorder (OCD). This brain region is part of several neural circuits, including the orbitofronto-striatal circuit and dorsolateral prefronto-striatal circuit. There are, however, no published studies investigating those circuits at a network level in non-medicated patients with OCD. Resting state functional magnetic resonance imaging scans were obtained from 20 non-medicated patients with OCD and 23 matched healthy volunteers. Voxelwise statistical parametric maps testing strength of functional connectivity of three striatal seed regions of interest (ROIs) with remaining brain regions were calculated and compared between groups. We performed additional correlation analyses between strength of connectivity and the severity scores for obsessive-compulsive symptoms, depression, and anxiety in the OCD group. Positive functional connectivity with the ventral striatum was significantly increased (Pcorrected <.05) in the orbitofrontal cortex, ventral medial prefrontal cortex and dorsal lateral prefrontal cortex of subjects with OCD. There was no significant correlation between measures of symptom severity and the strength of connectivity (Puncorrected <.001). This is the first study to investigate the corticostriatal connectivity in non-medicated patients with OCD. These findings provide the first direct evidence supporting a pathophysiological model involving basal ganglia circuitry in OCD.

Keywords

Obsessive-compulsive disorderFunctional magnetic resonance imagingResting stateFunctional connectivityBasal gangliaOrbitofrontal cortex
Type
Original article
Information
European Psychiatry , Volume 26 , Issue 7 , October 2011 , pp. 463 - 469
Copyright
Copyright © European Psychiatric Association 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

☆

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. All authors had full access to the data used in this study and corresponding author Yuki Sakai takes responsibility for the integrity of the data and the accuracy of the data analysis.

References

Adler, C.M.McDonough-Ryan, P.Sax, K.W.Holland, S.K.Arndt, S.Strakowski, S.M.fMRI of neuronal activation with symptom provocation in unmedicated patients with obsessive compulsive disorder. J Psychiatr Res 344–52000 317–324CrossRefGoogle ScholarPubMed
Alexander, G.E.DeLong, M.R.Strick, P.L.Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986; 9: 357–381CrossRefGoogle ScholarPubMed
Anand, A.Li, Y.Wang, Y.Wu, J.Gao, S.Bukhari, L.et al.Antidepressant effect on connectivity of the mood-regulating circuit: an FMRI study. Neuropsychopharmacology 2005; 30(7): 1334–1344CrossRefGoogle ScholarPubMed
Baxter, L.R. Jr.Phelps, M.E.Mazziotta, J.C.Guze, B.H.Schwartz, J.M.Selin, C.E.Local cerebral glucose metabolic rates in obsessive-compulsive disorder. A comparison with rates in unipolar depression and in normal controls. Arch Gen Psychiatry 1987; 44(3): 211–218CrossRefGoogle ScholarPubMed
Birn, R.M.Diamond, J.B.Smith, M.A.Bandettini, P.A.Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 2006; 31(4): 1536–1548CrossRefGoogle ScholarPubMed
Biswal, B.Yetkin, F.Z.Haughton, V.M.Hyde, J.S.Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 1995; 34(4): 537–541CrossRefGoogle ScholarPubMed
Broyd, S.J.Demanuele, C.Debener, S.Helps, S.K.James, C.J.Sonuga-Barke, E.J.Default-mode brain dysfunction in mental disorders: a systematic review. Neurosci Biobehav Rev 2009; 33(3): 279–296CrossRefGoogle ScholarPubMed
Chamberlain, S.R.Fineberg, N.A.Menzies, L.A.Blackwell, A.D.Bullmore, E.T.Robbins, T.W.et al.Impaired cognitive flexibility and motor inhibition in unaffected first-degree relatives of patients with obsessive-compulsive disorder. Am J Psychiatry 2007; 164(2): 335–338CrossRefGoogle ScholarPubMed
Chamberlain, S.R.Menzies, L.Hampshire, A.Suckling, J.Fineberg, N.A.del Campo, N.et al.Orbitofrontal dysfunction in patients with obsessive-compulsive disorder and their unaffected relatives. Science 2008; 321(5887): 421–422CrossRefGoogle ScholarPubMed
Damoiseaux, J.S.Rombouts, S.A.Barkhof, F.Scheltens, P.Stam, C.J.Smith, S.M.et al.Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 2006; 103(37): 13848–13853CrossRefGoogle ScholarPubMed
Di Martino, A.Scheres, A.Margulies, D.S.Kelly, A.M.Uddin, L.Q.Shehzad, Z.et al.Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 2008; 18(12): 2735–2747CrossRefGoogle ScholarPubMed
First, M.B.Spizer, R.L.Gibbon, M.Williams, J.B.W.Structures Clinical Interview for Axis I DSM-IV Disorders-Patient Edition (CID-I/P). New York: Biometrics Research Department, New York State Psychiatric Institute: 1994Google Scholar
First, M.B.Spizer, R.L.Gibbon, M.Williams, J.B.W.Structures Clinical Interview for DSM IV TR Axis I Disorders-Non-patient Edition (SCID-I/NP). New York: Biometrics Research Department, New York State Psychiatric Institute: 2001Google Scholar
Friedman, D.P.Aggleton, J.P.Saunders, R.C.Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: combined anterograde and retrograde tracing study in the Macaque brain. J Comp Neurol 2002; 450(4): 345–365CrossRefGoogle ScholarPubMed
Greicius, M.D.Krasnow, B.Reiss, A.L.Menon, V.Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 2003; 100(1): 253–258CrossRefGoogle ScholarPubMed
Haber, S.N.The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 2003; 26(4): 317–330CrossRefGoogle ScholarPubMed
Hamilton, M.The assessment of anxiety states by rating. Br J Med Psychol 1959; 32(1): 50–55CrossRefGoogle ScholarPubMed
Hamilton, M.Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol 1967; 6(4): 278–296CrossRefGoogle ScholarPubMed
Hampshire, A.Owen, A.M.Fractionating attentional control using event-related fMRI. Cereb Cortex 2006; 16(12): 1679–1689CrossRefGoogle ScholarPubMed
Harrison, B.J.Soriano-Mas, C.Pujol, J.Ortiz, H.Lopez-Sola, M.Hernandez-Ribas, R.et al.Altered corticostriatal functional connectivity in obsessive-compulsive disorder. Arch Gen Psychiatry 2009; 66(11): 1189–1200CrossRefGoogle ScholarPubMed
Jang, J.H.Kim, J.H.Jung, W.H.Choi, J.S.Jung, M.H.Lee, J.M.et al.Functional connectivity in fronto-subcortical circuitry during the resting state in obsessive-compulsive disorder. Neurosci Lett 2010; 474(3): 158–162CrossRefGoogle Scholar
Leopold, D.A.Murayama, Y.Logothetis, N.K.Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb Cortex 2003; 13(4): 422–433CrossRefGoogle ScholarPubMed
Lowe, M.J.Mock, B.J.Sorenson, J.A.Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 1998; 7(2): 119–132CrossRefGoogle ScholarPubMed
Macey, P.M.Macey, K.E.Kumar, R.Harper, R.M.A method for removal of global effects from fMRI time series. Neuroimage 2004; 22(1): 360–366CrossRefGoogle ScholarPubMed
Maltby, N.Tolin, D.F.Worhunsky, P.O’Keefe, T.M.Kiehl, K.A.Dysfunctional action monitoring hyperactivates frontal-striatal circuits in obsessive-compulsive disorder: an event-related fMRI study. Neuroimage 2005; 24(2): 495–503CrossRefGoogle Scholar
Mataix-Cols, D.Wooderson, S.Lawrence, N.Brammer, M.J.Speckens, A.Phillips, M.L.Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Arch Gen Psychiatry 2004; 61(6): 564–576CrossRefGoogle ScholarPubMed
Menzies, L.Chamberlain, S.R.Laird, A.R.Thelen, S.M.Sahakian, B.J.Bullmore, E.T.Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neurosci Biobehav Rev 2008; 32(3): 525–549CrossRefGoogle ScholarPubMed
Murphy, K.Birn, R.M.Handwerker, D.A.Jones, T.B.Bandettini, P.A.The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 2009; 44(3): 893–905CrossRefGoogle ScholarPubMed
Nagahama, Y.Okada, T.Katsumi, Y.Hayashi, T.Yamauchi, H.Oyanagi, C.et al.Dissociable mechanisms of attentional control within the human prefrontal cortex. Cereb Cortex 2001; 11(1): 85–92CrossRefGoogle ScholarPubMed
Nakajima, T.Nakamura, M.Taga, C.Yamagami, S.Kiriike, N.Nagata, T.et al.Reliability and validity of the Japanese version of the Yale-Brown Obsessive-Compulsive Scale. Psychiatry Clin Neurosci 1995; 49(2): 121–126CrossRefGoogle ScholarPubMed
O’Doherty, J.Dayan, P.Schultz, J.Deichmann, R.Friston, K.Dolan, R.J.Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 2004; 304(5669): 452–454CrossRefGoogle ScholarPubMed
O’Donnell, P.Grace, A.A.Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci 155 Pt 11995 3622–3639CrossRefGoogle ScholarPubMed
Pigott, T.A.Seay, S.M.A review of the efficacy of selective serotonin reuptake inhibitors in obsessive-compulsive disorder. J Clin Psychiatry 1999; 60(2): 101–106CrossRefGoogle ScholarPubMed
Rauch, S.L.Jenike, M.A.Alpert, N.M.Baer, L.Breiter, H.C.Savage, C.R.et al.Regional cerebral blood flow measured during symptom provocation in obsessive-compulsive disorder using oxygen 15-labeled carbon dioxide and positron emission tomography. Arch Gen Psychiatry 1994; 51(1): 62–70CrossRefGoogle ScholarPubMed
Saxena, S.Brody, A.L.Schwartz, J.M.Baxter, L.R.Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. Br J Psychiatry Suppl 1998; 35: 26–37CrossRefGoogle Scholar
Schwarz, A.J.Gozzi, A.Reese, T.Bifone, A.In vivo mapping of functional connectivity in neurotransmitter systems using pharmacological MRI. Neuroimage 2007; 34(4): 1627–1636CrossRefGoogle ScholarPubMed
Tanaka, S.C.Schweighofer, N.Asahi, S.Shishida, K.Okamoto, Y.Yamawaki, S.et al.Serotonin differentially regulates short- and long-term prediction of rewards in the ventral and dorsal striatum. PLoS One 2007; 2(12): e1333CrossRefGoogle Scholar
van den Heuvel, O.A.Veltman, D.J.Groenewegen, H.J.Cath, D.C.van Balkom, A.J.van Hartskamp, J.et al.Frontal-striatal dysfunction during planning in obsessive-compulsive disorder. Arch Gen Psychiatry 2005; 62(3): 301–309CrossRefGoogle ScholarPubMed
Ward BD. Simultaneous inference for FMRI data. 2000. http://afni.nimh.nih.gov/afni/doc/manual/AlphaSim.Google Scholar
Weissman, M.M.Bland, R.C.Canino, G.J.Greenwald, S.Hwu, H.G.Lee, C.K.et al.The cross national epidemiology of obsessive compulsive disorder. J Clin Psychiatry 55Suppl.1994 5–10Google ScholarPubMed
Whiteside, S.P.Port, J.D.Abramowitz, J.S.A meta-analysis of functional neuroimaging in obsessive-compulsive disorder. Psychiatry Res 2004; 132(1): 69–79CrossRefGoogle ScholarPubMed
Zhou, Y.Shu, N.Liu, Y.Song, M.Hao, Y.Liu, H.et al.Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr Res 1001–32008 120–132CrossRefGoogle Scholar
Submit a response

Comments

No Comments have been published for this article.