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The neural correlates of self-paced finger tapping in bipolar depression with motor retardation

Published online by Cambridge University Press:  22 February 2013

Benny Liberg ,
Mats Adler ,
Tomas Jonsson ,
Mikael Landén ,
Christoffer Rahm ,
Lars-Olof Wahlund ,
Maria Kristoffersen-Wiberg  and
Björn Wahlund
Benny Liberg*
Affiliation:
Department of Clinical Neuroscience, Division of Psychiatry, Karolinska Institutet, Stockholm, Sweden
Mats Adler
Affiliation:
Department of Clinical Neuroscience, Division of Psychiatry, Karolinska Institutet, Stockholm, Sweden
Tomas Jonsson
Affiliation:
Department of Diagnostic Medical Physics, Karolinska University Hospital Huddinge, Stockholm, Sweden
Mikael Landén
Affiliation:
Department of Clinical Neuroscience, Division of Psychiatry, Karolinska Institutet, Stockholm, Sweden Institute of Neuroscience and Physiology, University of Gothenburg, Gothenburg, Sweden
Christoffer Rahm
Affiliation:
Department of Clinical Neuroscience, Division of Psychiatry, Karolinska Institutet, Stockholm, Sweden
Lars-Olof Wahlund
Affiliation:
Department of Neurobiology, Care Sciences and Society, Division of Clinical Geriatrics, Karolinska University Hospital, Stockholm, Sweden
Maria Kristoffersen-Wiberg
Affiliation:
Department of Clinical Science, Intervention and Technology, Division of Medical Imaging and Technology, Karolinska Institutet, Stockholm, Sweden
Björn Wahlund
Affiliation:
Department of Clinical Neuroscience, Division of Psychiatry, Karolinska Institutet, Stockholm, Sweden Department of Energy and Engineering, Swedish University of Agricultural Sciences, Uppsala, Sweden
*
Benny Liberg, Department of Clinical Neuroscience, Division of Psychiatry, Karolinska Institutet, Psykiatri Sydväst, M 58, Karolinska University Hospital Huddinge, 141 86 Stockholm, Sweden. Tel: +46(0)702423076; Fax: +46(0)7795416; E-mail: [email protected]
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Abstract

Objective

Motor retardation is a characteristic feature of bipolar depression, and is also a core feature of Parkinson's disease. Within the framework of the functional deafferentiation theory in Parkinson's disease, we hypothesised that motor retardation in bipolar depression is mediated by disrupted subcortical activation, leading to decreased activation of cortical motor areas during finger tapping.

Methods

We used functional magnetic resonance imaging to investigate neural activity during self-paced finger tapping to elucidate whether brain regions that mediate preparation, control and execution of movement are activated differently in subjects with bipolar depression (n = 9) compared to healthy controls (n = 12).

Results

An uncorrected whole-brain analysis revealed significant group differences in dorsolateral and ventromedial prefrontal cortex. Corrected analyses showed non-significant differences in patients compared to controls: decreased and less widespread activation of the left putamen and left pallidum; increased activity in the left thalamus and supplementary motor area; decreased activation in the left lateral pre- and primary motor cortices; absence of activation in the pre-supplementary motor area; activation of the bilateral rostral cingulate motor area.

Conclusion

Both movement preparation and execution may be affected in motor retardation, and the activity in the whole left-side motor circuit is altered during self-initiated motor performance in bipolar depression.

Keywords

magnetic resonance imagingmood disorderParkinson diseasepsychomotor performance
Type
Original Articles
Information
Acta Neuropsychiatrica , Volume 25 , Issue 1 , February 2013 , pp. 43 - 51
Copyright
Scandinavian College of Neuropsychopharmacology 2013

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References

1Mitchell, PB, Malhi, GS.Bipolar depression: phenomenological overview and clinical characteristics. Bipolar Disord 2004;6:530–539.CrossRefGoogle ScholarPubMed
2Mitchell, PB, Wilhelm, K, Parker, G, Austin, MP, Rutgers, P, Malhi, GS.The clinical features of bipolar depression: a comparison with matched major depressive disorder patients. J Clin Psychiatry 2001;62:212–216, quiz 217.CrossRefGoogle ScholarPubMed
3Austin, MP, Mitchell, P, Hadzi-Pavlovic, Det al.Effect of apomorphine on motor and cognitive function in melancholic patients: a preliminary report. Psychiatry Res 2000;97:207–215.CrossRefGoogle ScholarPubMed
4Schrijvers, D, Hulstijn, W, Sabbe, BG.Psychomotor symptoms in depression: a diagnostic, pathophysiological and therapeutic tool. J Affect Disord 2008;109:1–20.CrossRefGoogle ScholarPubMed
5Buyukdura, JS, McClintock, SM, Croarkin, PE.Psychomotor retardation in depression: biological underpinnings, measurement, and treatment. Prog Neuropsychopharmacol Biol Psychiatry 2011;35:395–409.CrossRefGoogle ScholarPubMed
6Calugi, S, Cassano, GB, Litta, Aet al.Does psychomotor retardation define a clinically relevant phenotype of unipolar depression?. J Affect Disord 2011;129:296–300.CrossRefGoogle ScholarPubMed
7Mah, L, Zarate, CA Jr.Nugent, AC, Singh, JB, Manji, HK, Drevets, WC.Neural mechanisms of antidepressant efficacy of the dopamine receptor agonist pramipexole in treatment of bipolar depression. Int J Neuropsychopharmacol 2011;14:545–551.CrossRefGoogle ScholarPubMed
8Sobin, C, Sackeim, HA.Psychomotor symptoms of depression. Am J Psychiatry 1997;154:4–17.Google ScholarPubMed
9Caligiuri, MP, Brown, GG, Meloy, MJet al.An fMRI study of affective state and medication on cortical and subcortical brain regions during motor performance in bipolar disorder. Psychiatry Res 2003;123:171–182.CrossRefGoogle ScholarPubMed
10Caligiuri, MP, Brown, GG, Meloy, MJet al.A functional magnetic resonance imaging study of cortical asymmetry in bipolar disorder. Bipolar Disord 2004;6:183–196.CrossRefGoogle ScholarPubMed
11Dewey, RB Jr.Hutton, JT, LeWitt, PA, Factor, SA.A randomized, double-blind, placebo-controlled trial of subcutaneously injected apomorphine for parkinsonian off-state events. Arch Neurol 2001;58:1385–1392.CrossRefGoogle ScholarPubMed
12Kano, O, Ikeda, K, Kiyozuka, Tet al.Beneficial effect of pramipexole for motor function and depression in Parkinson's disease. Neuropsychiatr Dis Treat 2008;4:707–710.Google ScholarPubMed
13DeLong, MR, Wichmann, T.Circuits and circuit disorders of the basal ganglia. Arch Neurol 2007;64:20–24.CrossRefGoogle ScholarPubMed
14DeLong, M, Wichmann, T.Changing views of basal ganglia circuits and circuit disorders. Clin EEG Neurosci 2010;41:61–67.CrossRefGoogle ScholarPubMed
15Dagher, A, Nagano-Saito, A.Functional and anatomical magnetic resonance imaging in Parkinson's disease. Mol Imaging Biol 2007;9:234–242.CrossRefGoogle ScholarPubMed
16Asberg, M, Montgomery, SA, Perris, C, Schalling, D, Sedvall, G.A comprehensive psychopathological rating scale. Acta Psychiatr Scand Suppl 1978;271:5–27.CrossRefGoogle Scholar
17Hickie, I, Mason, C, Parker, G.Comparative validity of two measures of psychomotor function in patients with severe depression. J Affect Disord 1996;37:143–149.CrossRefGoogle ScholarPubMed
18Sweeney, JE, Slade, HP, Ivins, RG, Nemeth, DG, Ranks, DM, Sica, RB.Scientific investigation of brain-behavior relationships using the Halstead-Reitan Battery. Appl Neuropsychol 2007;14:65–72.CrossRefGoogle ScholarPubMed
26Worsley, KJ.Statistical analysis of activation images. In: Jezzard, PMatthews, PMSmith, SM, eds.Functional MRI: an introduction to methods, 1st edn. Oxford, UK: OUP, 2001.Google Scholar
20Desikan, RS, Segonne, F, Fischl, Bet al.An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006;31:968–980.CrossRefGoogle ScholarPubMed
21Geyer, S, Ledberg, A, Schleicher, Aet al.Two different areas within the primary motor cortex of man. Nature 1996;382:805–807.CrossRefGoogle ScholarPubMed
22Geyer, S.The microstructural border between the motor and the cognitive domain in the human cerebral corte. Adv Anat Embryol Cell Biol 2004;174:I–VIII, 1–89.Google Scholar
23Patenaude, B, Smith, SM, Kennedy, DN, Jenkinson, M.A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 2011;56:907–922.CrossRefGoogle ScholarPubMed
24Jenkinson, M, Bannister, P, Brady, M, Smith, S.Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002;17:825–841.CrossRefGoogle ScholarPubMed
25Smith, SM.Fast robust automated brain extraction. Hum Brain Mapp 2002;17:143–155.CrossRefGoogle ScholarPubMed
26Woolrich, MW, Ripley, BD, Brady, M, Smith, SM.Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 2001;14:1370–1386.CrossRefGoogle ScholarPubMed
27Jenkinson, M, Smith, S.A global optimisation method for robust affine registration of brain images. Med Image Anal 2001;5:143–156.CrossRefGoogle ScholarPubMed
28Andersson, J.Non-linear registration aka spatial normalisation FMRIB technial report TR07JA2. FMRIB Analysis Group Technical Reports. Oxford: FMRIB, 2007: 22.Google Scholar
29Woolrich, MW, Jbabdi, S, Patenaude, Bet al.Bayesian analysis of neuroimaging data in FSL. Neuroimage 2009; 45:S173–186.CrossRefGoogle ScholarPubMed
30Woolrich, MW, Behrens, TE, Beckmann, CF, Jenkinson, M, Smith, SM.Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 2004;21:1732–1747.CrossRefGoogle ScholarPubMed
31Woolrich, M.Robust group analysis using outlier inference. Neuroimage 2008;41:286–301.CrossRefGoogle ScholarPubMed
32Beckmann, CF, Jenkinson, M, Smith, SM.General multilevel linear modeling for group analysis in FMRI. Neuroimage 2003;20:1052–1063.CrossRefGoogle Scholar
33Dolan, RJ, Bench, CJ, Liddle, PFet al.Dorsolateral prefrontal cortex dysfunction in the major psychoses; symptom or disease specificity? J Neurol Neurosurg Psychiatry 1993;56:1290–1294.CrossRefGoogle ScholarPubMed
34Mayberg, HS, Lewis, PJ, Regenold, W, Wagner, HN Jr.Paralimbic hypoperfusion in unipolar depression. J Nucl Med 1994;35:929–934.Google ScholarPubMed
35Bench, CJ, Friston, KJ, Brown, RG, Frackowiak, RS, Dolan, RJ.Regional cerebral blood flow in depression measured by positron emission tomography: the relationship with clinical dimensions. Psychol Med 1993;23:579–590.CrossRefGoogle ScholarPubMed
36Videbech, P, Ravnkilde, B, Pedersen, THet al.The Danish PET/depression project: clinical symptoms and cerebral blood flow. A regions-of-interest analysis. Acta Psychiatr Scand 2002;106:35–44.CrossRefGoogle ScholarPubMed
37Meyer, JH, Kruger, S, Wilson, AAet al.Lower dopamine transporter binding potential in striatum during depression. Neuroreport 2001;12:4121–4125.CrossRefGoogle ScholarPubMed
38Meyer, JH, McNeely, HE, Sagrati, Set al.Elevated putamen D(2) receptor binding potential in major depression with motor retardation: an [11C]raclopride positron emission tomography study. Am J Psychiatry 2006;163: 1594–1602.CrossRefGoogle ScholarPubMed
39Caligiuri, MP, Brown, GG, Meloy, MJ, Eberson, S, Niculescu, AB, Lohr, JB.Striatopallidal regulation of affect in bipolar disorder. J Affect Disord 2006;91:235–242.CrossRefGoogle ScholarPubMed
40Marchand, WR, Lee, JN, Thatcher, GWet al.A functional MRI study of a paced motor activation task to evaluate frontal-subcortical circuit function in bipolar depression. Psychiatry Res 2007;155:221–230.CrossRefGoogle ScholarPubMed
41Marchand, WR, Lee, JN, Thatcher, J, Thatcher, GW, Jensen, C, Starr, J.A preliminary longitudinal fMRI study of frontal-subcortical circuits in bipolar disorder using a paced motor activation paradigm. J Affect Disord 2007;103:237–241.CrossRefGoogle ScholarPubMed
42Miller, EK, Cohen, JD.An integrative theory of prefrontal cortex function. Annu Rev Neurosci 2001;24:167–202.CrossRefGoogle ScholarPubMed
43Keedwell, PA, Andrew, C, Williams, SC, Brammer, MJ, Phillips, ML.The neural correlates of anhedonia in major depressive disorder. Biol Psychiatry 2005;58:843–853.CrossRefGoogle ScholarPubMed
44Kringelbach, ML.The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci 2005;6:691–702.CrossRefGoogle ScholarPubMed
45Brooks, DJ.Functional imaging of Parkinson's disease: is it possible to detect brain areas for specific symptoms? J Neural Transm Suppl 1999;56:139–153.CrossRefGoogle ScholarPubMed
46Ceballos-Baumann, AO.Functional imaging in Parkinson's disease: activation studies with PET, fMRI and SPECT. J Neurol 2003;250(Suppl. 1):I15–123.CrossRefGoogle ScholarPubMed
47Grafton, ST.Contributions of functional imaging to understanding parkinsonian symptoms. Curr Opin Neurobiol 2004;14:715–719.CrossRefGoogle ScholarPubMed
48Shimoyama, I, Ninchoji, T, Uemura, K.The finger-tapping test. A quantitative analysis. Arch Neurol 1990;47:681–684.CrossRefGoogle ScholarPubMed
49Witt, ST, Laird, AR, Meyerand, ME.Functional neuroimaging correlates of finger-tapping task variations: an ALE meta-analysis. Neuroimage 2008;42:343–356.CrossRefGoogle ScholarPubMed
50Allison, JD, Meador, KJ, Loring, DW, Figueroa, RE, Wright, JC.Functional MRI cerebral activation and deactivation during finger movement. Neurology 2000;54: 135–142.CrossRefGoogle ScholarPubMed
51Adler, M, Liberg, B, Andersson, S, Isacsson, G, Hetta, J.Development and validation of the affective self rating scale for manic, depressive, and mixed affective states. Nord J Psychiatry 2008;62:130–135.CrossRefGoogle ScholarPubMed