Frontostriatal functional connectivity in major depressive disorder

Biology of Mood & Anxiety Disorders

Daniella J Furman¹  J Paul Hamilton¹  Ian H Gotlib¹ 

[1] Department of Psychology, Stanford University, 450 Serra Mall, Stanford, CA 94305-2004, USA

关键词: fMRI;    dorsolateral prefrontal cortex;    subgenual anterior cingulate cortex;    striatum;    functional connectivity;    depression;   

Others  :  794444
DOI  :  10.1186/2045-5380-1-11

 received in 2011-07-13, accepted in 2011-12-08,  发布年份 2011

【 摘 要 】

Background

Abnormalities of the striatum and frontal cortex have been reported consistently in studies of neural structure and function in major depressive disorder (MDD). Despite speculation that compromised connectivity between these regions may underlie symptoms of MDD, little work has investigated the integrity of frontostriatal circuits in this disorder.

Methods

Functional magnetic resonance images were acquired from 21 currently depressed and 19 never-disordered women during wakeful rest. Using four predefined striatal regions-of-interest, seed-to-whole brain correlations were computed and compared between groups.

Results

Compared to controls, depressed participants exhibited attenuated functional connectivity between the ventral striatum and both ventromedial prefrontal cortex and subgenual anterior cingulate cortex. Depressed participants also exhibited stronger connectivity between the dorsal caudate and dorsal prefrontal cortex, which was positively correlated with severity of the disorder.

Conclusions

Depressed individuals are characterized by aberrant connectivity in frontostriatal circuits that are posited to support affective and cognitive processing. Further research is required to examine more explicitly the link between patterns of disrupted connectivity and specific symptoms of depression, and the extent to which these patterns precede the onset of depression and normalize with recovery from depressive illness.

【 授权许可】

   
2011 Furman et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Kessler RC, Wang PS: Epidemiology of Depression. In Handbook of Depression. 2nd edition. Edited by Gotlib IH, Hammen CL. New York: The Guilford Press; 2009:5-22.
• [2]Gotlib IH, Joormann J: Cognition and depression: current status and future directions. Annu Rev Clin Psychol 2010, 6:285-312.
• [3]Videbach P: PET measurements of brain glucose metabolism and blood flow in major depressive disorder: a critical review. Acta Psychiatr Scand 2000, 101:11-20.
• [4]Dunn RT, Kimbrell TA, Ketter TA, Frye MA, Willis MW, Luckenbaugh DA, Post RM: Principal components of the beck depression inventory and regional cerebral metabolism in unipolar and bipolar depression. Biol Psychiatry 2002, 51:387-399.
• [5]Mink JW: The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 1996, 50:381-425.
• [6]Grillner S, Hellgren J, Ménard A, Saitoh K, Wilström : Mechanisms for selection of basic motor programs - roles for the striatum and pallidum. Trends Neurosci 2005, 28:364-370.
• [7]Frank MJ, Loughry B, O'Reilly RC: Interactions between frontal cortex and basal ganglia in working memory: a computational model. Cogn Affect Behav Neurosci 2001, 1:137-160.
• [8]Alexander GE, DeLong MR, Strick PL: Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci 1986, 9:357-381.
• [9]Haber SN, Fudge JL, McFarland NR: Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 2000, 20:2369-2382.
• [10]Marchand WR: Cortico-basal ganglia circuitry: a review of key research and implications for functional connectivity studies of mood and anxiety disorders. Brain Struct Funct 2010, 215:73-96.
• [11]Rogers MA, Bradshaw JL, Pantelis C, Phillips JG: Frontostriatal deficits in unipolar major depression. Brain Res Bull 1998, 47:297-310.
• [12]Heller AS, Johnstone T, Shackman AJ, Light SN, Peterson MJ, Kolden GG, Kalin NH, Davidson RJ: Reduced capacity to sustain positive emotion in major depression reflects diminished maintenance of fronto-striatal brain activation. Proc Natl Acad Sci USA 2009, 106:22445-22450.
• [13]Greicius M: Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol 2008, 21:424-430.
• [14]Di Martino A, Scheres A, Margulies DS, Kelly AM, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP: Functional connectivity of human striatum: a resting state fMRI study. Cereb Cortex 2008, 18:2735-2747.
• [15]Helmich RC, Derikx LC, Bakker M, Scheeringa R, Bloem BR, Toni I: Spatial remapping of cortiso-striatal connectivity in Parkinson's disease. Cereb Cortex 2010, 20:1175-1186.
• [16]Anand A, Li Y, Wang Y, Wu J, Gao S, Bukhari L, Mathews VP, Kalnin A, Lowe MJ: Activity and connectivity of brain mood rgulating circuit in depression: a functional magnetic resonance study. Biol Psychiatry 2005, 57:1079-1088.
• [17]Harrison NA, Brydon L, Walker C, Gray MA, Steptoe A, Critchley HD: Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity. Biol Psychiatry 2009, 66:407-414.
• [18]Cohen MX, Schoene-Bake J-C, Elger CE, Weber B: Connectivity-based segregation of the human striatum predicts personality characteristics. Nat Neurosci 2008, 12:32-34.
• [19]Nolen-Hoeksema S, Hilt LM: Gender differences in depression. In Handbook of Depression. 2nd edition. Edited by Gotlib IH, Hammen CL. New York, NY: Guilford Press; 2009:386-404.
• [20]Beck AT, Steer RA, Brown GK: Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation; 1996.
• [21]Nolen-Hoeksema S, Morrow J: A prospective study of depression and posttraumatic stress symptoms after a natural disaster: the 1989 Loma Prieta earthquake. J Pers Soc Psychol 1991, 61:115-121.
• [22]Glover GH, Law CS: Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn Reson Med 2001, 46:515-522.
• [23]Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, Smith SM, Beckmann CF, Adelstein JS, Buckner RL, Colcombe S, Dogonowski AM, Ernst M, Fair D, Hampson M, Hoptman MJ, Hyde JS, Kiviniemi VJ, Kötter R, Li SJ, Lin CP, Lowe MJ, Mackay C, Madden DJ, Madsen KH, Margulies DS, Mayberg HS, McMahon K, Monk CS, Mostofsky SH, Nagel BJ, et al.: Toward discovery science of human brain function. Proc Natl Acad Sci USA 2010, 107:4734-4739.
• [24]Kelly C, de Zubicaray G, Di Martino A, Copland DA, Reiss PT, Klein DF, Castellanos FX, Milham MP, McMahon K: l-Dopa modulates functional connectivity in striatal cognitive and motor networks: a double-blind placebo-controlled study. J Neurosci 2009, 29:7364-7378.
• [25]Chen G: Simple correlation analysis. [http://afni.nimh.nih.gov/sscc/gangc/SimCorrAna.html] webcite
• [26]Brett M: MRC CBU Imaging Wiki. [http://imaging.mrc-cbu.cam.ac.uk/imaging/MniTalairach] webcite
• [27]Ward BD: Simultaneous inference for fMRI data. [http://afni.nimh.nih.gov/afni/doc/manual/AlphaSim] webcite
• [28]Haber SN, Knutson B: The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010, 35:4-26.
• [29]Gotlib IH, Sivers H, Gabrieli JDE, Whitfield-Gabrieli S, Goldin P, Minor KL, Canli T: Subgenual anterior cingulate activation to valenced emotional stimuli in major depression. Neuroreport 2005, 16:1731-1734.
• [30]Pizzagalli DA, Iosifescu D, Hallett LA, Ratner KF, Fava M: Reduced hedonic capacity in major depressive disorder: evidence from a probabilistic reward task. J Psychiatr Res 2008, 43:76-87.
• [31]Beckmann M, Johansen-Berg H, Rushworth MFS: Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci 2009, 29:1175-1190.
• [32]Vogt BA: Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 2005, 6:533-544.
• [33]Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LLB, Parvizi J, Hichwa RD: Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 2000, 3:1049-1056.
• [34]Drevets WC, Price JL, Simpson JRS Jr, Todd RD, Reich T, Vannier M, Raichle ME: Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997, 386:824-827.
• [35]Ballmaier M, Toga AW, Blanton RE, Sowell ER, Lavretsky H, Peterson J, Pham D, Kumar A: Anterior cingulate, gyrus rectus, and orbitofrontal abnormalities in elderly depressed patients: an MRI-based parcellation of the prefrontal cortex. Am J Psychiatry 2004, 161:99-108.
• [36]Phillips ML, Drevets WC, Rauch SL, Lane R: Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol Psychiatry 2003, 54:504-514.
• [37]Fellows LK, Farah MJ: Ventromedial frontal cortex mediates affective shifting in humans: evidence from a reversal learning paradigm. Brain 2003, 126:1830-1837.
• [38]Knutson B, Fong GW, Charles MA, Varner JL, Hommer D: Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 2001, 12:3683-3687.
• [39]Wheeler EZ, Fellows LK: The human ventromedial frontal lobe is critical for learning from negative feedback. Brain 2008, 131:1323-1331.
• [40]Boecker H, Jankowski J, Ditter P, Scheef L: A role of the basal ganglia and midbrain nuclei for initiation of motor sequences. Neuroimage 2008, 39:1356-1369.
• [41]Pier MPBI, Hulstijn W, Sabbe BGC: Differential patterns of psychomotor functioning in unmedicated melancholic and nonmelancholic depressed patients. J Psychiatr Res 2004, 38:425-435.
• [42]Sabbe B, Hulstijn W, van Hoof J, Tuynman-Qua HG, Zitman F: Retardation in depression: assessment by means of simple motor tasks. J Affect Disord 1999, 55:39-44.
• [43]Rogers MA, Bradshaw JL, Phillips JG, Chiu E: Reliance on external cues during serial sequential movement in major depression. J Neurol Neurosurg Psychiatry 2000, 69:237-239.
• [44]Lewis SJG, Dove A, Robbins TW, Barker RA, Owen AM: Striatal contributions to working memory: a functional magnetic resonance imaging study in humans. Eur J Neurosci 2004, 19:755-760.
• [45]McNab F, Klingberg T: Prefrontal cortex and basal ganglia control access to working memory. Nat Neurosci 2008, 11:103-107.
• [46]Harvey PO, Le Bastard G, Pochon JB, Levy R, Allilaire JF, Dubois B, Fossati P: Executive functions and updating of the contents of working memory in unipolar depression. J Psychiatr Res 2004, 38:567-576.
• [47]Joormann J, Gotlib IH: Updating the contents of working memory in depression: interference from irrelevant negative material. J Abnorm Psychol 2008, 117:182-192.
• [48]Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL: A default mode of brain function. Proc Natl Acad Sci USA 2001, 98:676-682.
• [49]Gusnard DA, Akbudak E, Shulman GL, Raichle ME: Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci USA 2001, 98:4259-4264.
• [50]Sheline YI, Barch DM, Price JL, Rundle MM, Vaishnavi SN, Snyder AZ, Mintun MA, Wang S, Coalson RS, Raichle ME: The default mode network and self-referential processes in depression. Proc Natl Acad Sci USA 2009, 106:1942-1947.
• [51]Nagano-Saito A, Leyton M, Monchi O, Goldberg YK, He Y, Dagher A: Dopamine depletion impairs frontostriatal functional connectivity during a set-shifting task. J Neurosci 2008, 28:3697-3706.
• [52]van Eimeren T, Monchi O, Ballanger B, Strafella AP: Dysfunction of the default mode network in Parkinson disease: a functional magnetic resonance imaging study. Arch Neurol 2009, 66:877-883.
• [53]Anand A, Li Y, Wang Y, Wu J, Gao S, Bukhari L, Mathews VP, Kalnin A, Lowe MJ: Antidepressant effect on connectivity of the mood-regulating circuit: an fMRI study. Neuropsychopharmacology 2005, 30:1334-1344.
• [54]Bora E, Harrison BJ, Davey CG, Yücel M, Pantelis C: Meta-analysis of volumetric abnormalities in cortico-striatal-pallidal-thalamic circuits in major depressive disorder. Psychol Med, in press.
• [55]Kim MJ, Hamilton JP, Gotlib IH: Reduced caudate gray matter volume in women with major depressive disorder. Psychiat Res-Neuroim 2008, 164:114-122.
• [56]Parashos IA, Tupler LA, Blitchington T, Krishnan KRR: Magnetic-resonance morphometry in patients with major depression. Psychiat Res-Neuroim 1998, 84:7-15.