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Emotional processing and executive functions in major depressive disorder: dorsal prefrontal activity correlates with performance in the intra–extra dimensional set shift

Published online by Cambridge University Press:  24 June 2014

Alexander Heinzel ,
Georg Northoff ,
Heinz Boeker ,
Peter Boesiger  and
Simone Grimm
Alexander Heinzel*
Affiliation:
Department of Nuclear Medicine, University of Düsseldorf, Jülich, Germany
Georg Northoff
Affiliation:
Institute of Mental Health Research, University of Ottawa, Ottawa, Canada
Heinz Boeker
Affiliation:
Department of Psychiatry, University of Zurich, Zurich, Switzerland;
Peter Boesiger
Affiliation:
Institute of Biomedical Engineering, ETH and University of Zurich, Zurich, Switzerland
Simone Grimm
Affiliation:
Department of Psychiatry, University of Zurich, Zurich, Switzerland; Department of Psychiatry, Charité, Berlin, Germany Dahlem Institute for Neuroimaging of Emotion (DINE), Freie Universitaet Berlin, Germany
*
Alexander Heinzel, MD, Department of Nuclear Medicine, University of Düsseldorf at the Forschungszentrum Jülich, 52428 Jülich, Germany. Tel: +49 211 24616347; Fax: +492461618044; E-mail: [email protected]
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Abstract

Heinzel A, Northoff G, Boeker H, Boesiger P, Grimm S. Emotional processing and executive functions in major depressive disorder: dorsal prefrontal activity correlates with performance in the intra–extra dimensional set shift.

Objective:

Major depressive disorder (MDD) is characterised by predominately negatively valenced emotional symptoms that are often accompanied by cognitive impairments. We posited that cognitive impairments in MDD are related to altered emotional processing in prefrontal cortex.

Methods:

We compared 20 medication-free patients with MDD and 29 matched healthy controls. Both groups performed an emotional task during functional magnetic resonance imaging (fMRI). Furthermore, they completed the intra–extra dimensional set shift (IED) test probing for cognitive impairments. Then we correlated the results of the IED with the changes in fMRI BOLD signal in MDD patients and healthy subjects.

Results:

The subcategory of the IED applying extradimensional shift (EDS) showed a divergent performance of the MDD group committing significantly more errors than the control group. Correlating the EDS errors with fMRI signal changes, the healthy subjects showed a positive correlation with the right ventrolateral prefrontal cortex and the right orbitofrontal cortex. MDD subjects, in contrast, showed a positive correlation in right dorsolateral prefrontal cortex (DLPFC) and a negative correlation in the left dorsomedial prefrontal cortex (DMPFC).

Conclusion:

We hypothesise that the differential correlation in healthy controls and MDD patients may reflect the use of different strategies in their performance. The impaired executive functions, as reflected by altered processing in right DLPFC and left DMPFC, may implicitly influence emotional processing in patients suffering from MDD.

Keywords

mayor depressive disorderemotional processingexecutive functionsprefrontal cortexIEDfMRI
Type
Research Article
Information
Acta Neuropsychiatrica , Volume 22 , Issue 6 , December 2010 , pp. 269 - 279
Copyright
Copyright © 2010 John Wiley & Sons A/S

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References

Rimes, KA, Watkins, E.The effects of self-focused rumination on global negative self-judgements in depression. Behav Res Ther 2005;43:1673–1681.CrossRefGoogle ScholarPubMed
Raes, F, Hermans, D, Williams, JMet al. Is overgeneral autobiographical memory an isolated memory phenomenon in major depression? Memory 2006;14:584–594.CrossRefGoogle ScholarPubMed
Grimm, S, Boesiger, P, Beck, Jet al. Altered negative BOLD responses in the default-mode network during emotion processing in depressed subjects. Neuropsychopharmacology 2009;34:932–943.CrossRefGoogle ScholarPubMed
Levin, RL, Heller, W, Mohanty, Aet al. Cognitive deficits in depression and functional specificity of regional brain activity. Cogn Ther Res 2007;31:211–233.CrossRefGoogle Scholar
Damasio, AR.Descartes' error. New York: Avon Books, Inc., 1994.Google ScholarPubMed
Pessoa, L.On the relationship between emotion and cognition. Nat Rev Neurosci 2008;9:148–158.CrossRefGoogle ScholarPubMed
Baker, SC, Frith, CD, Dolan, RJ.The interaction between mood and cognitive function studied with PET. Psychol Med 1997;27:565–578.CrossRefGoogle ScholarPubMed
Bermpohl, F, Pascual-Leone, A, Amedi, Aet al. Attentional modulation of emotional stimulus processing: an fMRI study using emotional expectancy. Hum Brain Mapp 2006;27:662–677.CrossRefGoogle ScholarPubMed
Northoff, G, Heinzel, A, Bermpohl, Fet al. Reciprocal modulation and attenuation in the prefrontal cortex: an fMRI study on emotional-cognitive interaction. Hum Brain Mapp 2004;21:202–212.CrossRefGoogle Scholar
Northoff, G, Grimm, S, Boeker, Het al. Affective judgment and beneficial decision making: ventromedial prefrontal activity correlates with performance in the Iowa Gambling Task. Hum Brain Mapp 2006;27:572–587.CrossRefGoogle Scholar
Ochsner, KN, Ray, RD, Cooper, JCet al. For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. Neuroimage 2004;23: 483–499.CrossRefGoogle ScholarPubMed
Ochsner, KN, Gross, JJ.The cognitive control of emotion. Trends Cogn Sci 2005;9:242–249.CrossRefGoogle ScholarPubMed
Bartolic, EI, Basso, MR, Schefft, BKet al. Effects of experimentally-induced emotional states on frontal lobe cognitive task performance. Neuropsychologia 1999;37: 677–683.CrossRefGoogle ScholarPubMed
Elliott, R, Rubinsztein, JS, Sahakian, BJet al. The neural basis of mood-congruent processing biases in depression. Arch Gen Psychiatry 2002;59:597–604.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SLet al. Neurobiology of emotion perception II: implications for major psychiatric disorders. Biol Psychiatry 2003;54:515–528.CrossRefGoogle ScholarPubMed
Keedwell, PA, Andrew, C, Williams, SCet al. A double dissociation of ventromedial prefrontal cortical responses to sad and happy stimuli in depressed and healthy individuals. Biol Psychiatry 2005;58:495–503.CrossRefGoogle ScholarPubMed
Mayberg, HS.Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. Br Med Bull 2003;65:193–207.CrossRefGoogle ScholarPubMed
Surguladze, SA, Young, AW, Senior, Cet al. Recognition accuracy and response bias to happy and sad facial expressions in patients with major depression. Neuropsychology 2004;2:212–218.CrossRefGoogle Scholar
Grimm, S, Beck, J, Schuepbach, Det al. Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: an fMRI study in severe major depressive disorder. Biol Psychiatry 2008;63:369–376.CrossRefGoogle ScholarPubMed
Lawrence, NS, Williams, AM, Surguladze, Set al. Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biol Psychiatry 2004;55: 578–587.CrossRefGoogle ScholarPubMed
Goodwin, GM.Neuropsychological and neuroimaging evidence for the involvement of the frontal lobes in depression. J Psychopharmacol 1997;11:115–122.CrossRefGoogle ScholarPubMed
Veiel, HO.A preliminary profile of neuropsychological deficits associated with major depression. J Clin Exp Neuropsychol 1997;19:587–603.CrossRefGoogle ScholarPubMed
Austin, MP, Ross, M, Murray, Cet al. Cognitive function in major depression. J Affect Disord 1992;25:21–29.CrossRefGoogle ScholarPubMed
Elliott, R, Sahakian, BJ, Michael, Aet al. Abnormal neural response to feedback on planning and guessing tasks in patients with unipolar depression. Psychol Med 1998;28:559–571.CrossRefGoogle Scholar
Grant, MM, Thase, ME, Sweeney, JA.Cognitive disturbance in outpatient depressed younger adults: evidence of modest impairment. Biol Psychiatry 2001;50:35–43.CrossRefGoogle ScholarPubMed
Austin, MP, Mitchell, P, Wilhelm, Ket al. Cognitive function in depression: a distinct pattern of frontal impairment in melancholia? Psychol Med 1999;29:73–85.CrossRefGoogle ScholarPubMed
Beats, BC, Sahakian, BJ, Levy, R.Cognitive performance in tests sensitive to frontal lobe dysfunction in the elderly depressed. Psychol Med 1996;26:591–603.CrossRefGoogle ScholarPubMed
Murphy, FC, Sahakian, BJ, Rubinsztein, JSet al. Emotional bias and inhibitory control processes in mania and depression. Psychol Med 1999;29:1307–1321.CrossRefGoogle ScholarPubMed
Purcell, R, Maruff, P, Kyrios, Met al. Neuropsychological function in young patients with unipolar major depression. Psychol Med 1997;27:1277–1285.CrossRefGoogle ScholarPubMed
Dolan, 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
Elliott, R, Baker, SC, Rogers, RDet al. Prefrontal dysfunction in depressed patients performing a complex planning task: a study using positron emission tomography. Psychol Med 1997;27:931–942.CrossRefGoogle ScholarPubMed
Okada, G, Okamoto, Y, Morinobu, Set al. Attenuated left prefrontal activation during a verbal fluency task in patients with depression. Neuropsychobiology 2003;47:21–26.CrossRefGoogle ScholarPubMed
Fitzgerald, PB, Laird, AR, Maller, Jet al. A meta-analytic study of changes in brain activation in depression. Hum Brain Mapp 2008;29:683–695.CrossRefGoogle ScholarPubMed
Lang, PJ, Bradley, MM, Cuthbert, BN. International Affective Picture System (IAPS). Instruction manual and affective ratings. The Center for research in psychophysiology, University of Florida (Rep. No. A-4). Gainesville, Florida: University of California, 1999. Google Scholar
Robbins, TW, James, M, Owen, AMet al. Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. Dementia 1994;5:266–281.Google Scholar
Hamilton, M.A rating scale for depression. J Neurol Neurosurg Psychiatry 1960;23:56–62.CrossRefGoogle ScholarPubMed
Beck, AT.A systematic investigation of depression. Compr Psychiatry 1961;2:163–170.CrossRefGoogle ScholarPubMed
Lehrl, S, Triebig, G, Fischer, B.Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurol Scand 1995;91:335–345.CrossRefGoogle ScholarPubMed
Nelson, HE, O’Connell, A.Dementia: the estimation of premorbid intelligence levels using the New Adult Reading Test. Cortex 1978;14:234–244.CrossRefGoogle ScholarPubMed
Oldfield, RC.The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971;9:97–113.CrossRefGoogle Scholar
Grimm, S, Schmidt, CF, Bermpohl, Fet al. Segregated neural representation of distinct emotion dimensions in the prefrontal cortex – an fMRI study. Neuroimage 2006;30: 325–340.CrossRefGoogle ScholarPubMed
Stark, CE, Squire, LR.When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc Natl Acad Sci U S A 2001;98:12760–12766.CrossRefGoogle Scholar
Pruessmann, KP, Weiger, M, Scheidegger, MBet al. SENSE: sensitivity encoding for fast MRI. Magn Reson Med 1999;42:952–962.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Friston, KJ, Frith, CD, Turner, Ret al. Characterizing evoked hemodynamics with fMRI. Neuroimage 1995;2: 157–165.CrossRefGoogle ScholarPubMed
Friston, KJ, Holmes, AP, Poline, JBet al. Analysis of fMRI time-series revisited. Neuroimage 1995;2: 45–53.CrossRefGoogle ScholarPubMed
Anderson, AK, Christoff, K, Stappen, Iet al. Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 2003;6:196–202.CrossRefGoogle ScholarPubMed
Stordal, KI, Lundervold, AJ, Mykletun, Aet al. Frequency and characteristics of recurrent major depressed patients with unimpaired executive functions. World J Biol Psychiatry 2005;6:36–44.CrossRefGoogle ScholarPubMed
Beblo, T, Herrmann, M.Neuropsychological deficits in depressive disorders. Fortschr Neurol Psychiatr 2000;68: 1–11.CrossRefGoogle Scholar
Hammar, A.Automatic and effortful information processing in unipolar major depression. Scand J Psychol 2003;44:409–413.CrossRefGoogle ScholarPubMed
Den Hartog, HM, Nicolson, NA, Derix, MMet al. Salivary cortisol patterns and cognitive speed in major depression: a comparison with allergic rhinitis and healthy control subjects. Biol Psychol 2003;63:1–14.CrossRefGoogle ScholarPubMed
Tsourtos, G, Thompson, JC, Stough, C.Evidence of an early information processing speed deficit in unipolar major depression. Psychol Med 2002;32:259–265.CrossRefGoogle ScholarPubMed
Christensen, H, Griffiths, K, Mackinnon, Aet al. A quantitative review of cognitive deficits in depression and Alzheimer-type dementia. J Int Neuropsychol Soc 1997;3:631–651.CrossRefGoogle ScholarPubMed
Dias, R, Robbins, TW, Roberts, AC.Dissociable forms of inhibitory control within prefrontal cortex with an analog of the Wisconsin Card Sort Test: restriction to novel situations and independence from “on-line” processing. J Neurosci 1997;17:9285–9297.CrossRefGoogle ScholarPubMed
Dias, R, Robbins, TW, Roberts, AC.Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav Neurosci 1996;110:872–886.CrossRefGoogle ScholarPubMed
Rogers, RD, Andrews, TC, Grasby, PMet al. Contrasting cortical and subcortical activations produced by attentional-set shifting and reversal learning in humans. J Cogn Neurosci 2000;12:142–162.CrossRefGoogle ScholarPubMed
Goldman-Rakic, PS.Circuitry of primate prefrontal cortex and the organization of behavior by representational memory. In: Plum, F, Mountcastle, V, eds. Handbook of physiology. Bethesda: American Physiological Society, 1987. Google Scholar
Shafritz, KM, Kartheiser, P, Belger, A.Dissociation of neural systems mediating shifts in behavioral response and cognitive set. Neuroimage 2005;25:600–606.CrossRefGoogle ScholarPubMed
Konishi, S, Nakajima, K, Uchida, Iet al. Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 1999;122(Pt 5): 981–991.CrossRefGoogle ScholarPubMed
Smith, AB, Taylor, E, Brammer, Met al. Neural correlates of switching set as measured in fast, event-related functional magnetic resonance imaging. Hum Brain Mapp 2004;21:247–256.CrossRefGoogle ScholarPubMed
Phan, KL, Wager, T, Taylor, SFet al. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 2002;16: 331–348.CrossRefGoogle ScholarPubMed
Gusnard, DA, Akbudak, E, Shulman, GLet al. Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci U S A 2001;98:4259–4264.CrossRefGoogle ScholarPubMed
Lane, RD, Fink, GR, Chau, PMet al. Neural activation during selective attention to subjective emotional responses. Neuroreport 1997;8:3969–3972.CrossRefGoogle ScholarPubMed
Rogers, MA, Bellgrove, MA, Chiu, Eet al. Response selection deficits in melancholic but not nonmelancholic unipolar major depression. J Clin Exp Neuropsychol 2004;26:169–179.CrossRefGoogle Scholar
Staffen, W, Mair, A, Zauner, Het al. Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task. Brain 2002;125:1275–1282.CrossRefGoogle ScholarPubMed
Herwig, U, Baumgartner, T, Kaffenberger, Tet al. Modulation of anticipatory emotion and perception processing by cognitive control. Neuroimage 2007;37: 652–662.CrossRefGoogle ScholarPubMed
Phan, KL, Fitzgerald, DA, Nathan, PJet al. Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biol Psychiatry 2005;57:210–219.CrossRefGoogle ScholarPubMed
Phelps, EA, O’Connor, KJ, Gatenby, JCet al. Activation of the left amygdala to a cognitive representation of fear. Nat Neurosci 2001;4:437–441.CrossRefGoogle ScholarPubMed
Panksepp, J.Affective consciousness: core emotional feelings in animals and humans. Conscious Cogn 2005;14: 30–80.CrossRefGoogle ScholarPubMed