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Neural correlates of ‘pessimistic’ attitude in depression

Published online by Cambridge University Press:  07 September 2009

U. Herwig*
Affiliation:
Psychiatric University Hospital Zürich, Switzerland Department of Psychiatry, University of Ulm, Germany
A. B. Brühl
Affiliation:
Psychiatric University Hospital Zürich, Switzerland
T. Kaffenberger
Affiliation:
Psychiatric University Hospital Zürich, Switzerland Department of Psychiatry, University of Ulm, Germany
T. Baumgartner
Affiliation:
Department of Neuropsychology, University of Zürich, Switzerland Institute for Empirical Research in Economics, University of Zürich, Switzerland
H. Boeker
Affiliation:
Psychiatric University Hospital Zürich, Switzerland
L. Jäncke
Affiliation:
Department of Neuropsychology, University of Zürich, Switzerland
*
*Address for correspondence: U. Herwig, M.D., M.A., Psychiatric University Hospital, University of Zürich, Lenggstrasse 31, CH – 8032Zürich, Switzerland. (Email: uwe.herwig@puk.zh.ch)

Abstract

Background

Preparing for potentially threatening events in the future is essential for survival. Anticipating the future to be unpleasant is also a cognitive key feature of depression. We hypothesized that ‘pessimism’-related emotion processing would characterize brain activity in major depression.

Method

During functional magnetic resonance imaging, depressed patients and a healthy control group were cued to expect and then perceive pictures of known emotional valences – pleasant, unpleasant and neutral – and stimuli of unknown valence that could have been either pleasant or unpleasant. Brain activation associated with the ‘unknown’ expectation was compared with the ‘known’ expectation conditions.

Results

While anticipating pictures of unknown valence, activation patterns in depressed patients within the medial and dorsolateral prefrontal areas, inferior frontal gyrus, insula and medial thalamus were similar to activations associated with expecting unpleasant pictures, but not with expecting positive pictures. The activity within a majority of these areas correlated with the depression scores. Differences between healthy and depressed persons were found particularly for medial and dorsolateral prefrontal and insular activations.

Conclusions

Brain activation in depression during expecting events of unknown emotional valence was comparable with activation while expecting certainly negative, but not positive events. This neurobiological finding is consistent with cognitive models supposing that depressed patients develop a ‘pessimistic’ attitude towards events with an unknown emotional meaning. Thereby, particularly the role of brain areas associated with the processing of cognitive and executive control and of the internal state is emphasized in contributing to major depression.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2009

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References

Abler, B, Erk, S, Herwig, U, Walter, H (2006). Anticipation of aversive stimuli activates extended amygdala in unipolar depression. Journal of Psychiatric Research 41, 511522.CrossRefGoogle ScholarPubMed
Anderson, AK, Christoff, K, Stappen, I, Panitz, D, Ghahremani, DG, Glover, G, Gabrieli, JD, Sobel, N (2003). Dissociated neural representations of intensity and valence in human olfaction. Nature Neuroscience 6, 196202.CrossRefGoogle ScholarPubMed
Annett, M (1967). The binomial distribution of right, mixed and left handedness. Quarterly Journal of Experimental Psychology 19, 327333.CrossRefGoogle ScholarPubMed
Baxter, LR Jr, Schwartz, JM, Phelps, ME, Mazziotta, JC, Guze, BH, Selin, CE, Gerner, RH, Sumida, RM (1989). Reduction of prefrontal cortex glucose metabolism common to three types of depression. Archives of General Psychiatry 46, 243250.CrossRefGoogle ScholarPubMed
Beck, AT (1967). Depression: Clinical, Experimental and Theoretical Aspects. Harper & Row: New York.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561571.CrossRefGoogle ScholarPubMed
Bermpohl, F, Pascual-Leone, A, Amedi, A, Merabet, LB, Fregni, F, Gaab, N, Alsop, D, Schlaug, G, Northoff, G (2006). Dissociable networks for the expectancy and perception of emotional stimuli in the human brain. NeuroImage 30, 588600.CrossRefGoogle ScholarPubMed
Calder, AJ, Lawrence, AD, Young, AW (2001). Neuropsychology of fear and loathing. Nature Reviews Neuroscience 2, 352363.CrossRefGoogle Scholar
Carter, CS, Macdonald, AM, Botvinick, M, Ross, LL, Stenger, VA, Noll, D, Cohen, JD (2000). Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. Proceedings of the National Academy of Sciences of the USA 97, 19441948.CrossRefGoogle ScholarPubMed
Churchland, PS (2002). Self-representation in nervous systems. Science 296, 308310.CrossRefGoogle ScholarPubMed
Craig, AD (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience 3, 655666.CrossRefGoogle Scholar
Critchley, HD, Wiens, S, Rotshtein, P, Ohman, A, Dolan, RJ (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience 7, 189195.CrossRefGoogle ScholarPubMed
Damasio, AR, Grabowski, TJ, Bechara, A, Damasio, H, Ponto, LL, Parvizi, J, Hichwa, RD (2000). Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience 3, 10491056.CrossRefGoogle ScholarPubMed
Dannlowski, U, Ohrmann, P, Bauer, J, Deckert, J, Hohoff, C, Kugel, H, Arolt, V, Heindel, W, Kersting, A, Baune, BT, Suslow, T (2008). 5-HTTLPR biases amygdala activity in response to masked facial expressions in major depression. Neuropsychopharmacology 33, 418424.CrossRefGoogle ScholarPubMed
Davidson, RJ, Irwin, W, Anderle, MJ, Kalin, NH (2003). The neural substrates of affective processing in depressed patients treated with venlafaxine. American Journal of Psychiatry 160, 6475.CrossRefGoogle ScholarPubMed
Davidson, RJ, Pizzagalli, D, Nitschke, JB, Putnam, K (2002). Depression: perspectives from affective neuroscience. Annual Reviews of Psychology 53, 545574.CrossRefGoogle ScholarPubMed
Drevets, WC (2001). Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders. Current Opinions in Neurobiology 11, 240249.CrossRefGoogle ScholarPubMed
Erk, S, Walter, H, Abler, B (2008). Age-related physiological responses to emotion anticipation and exposure. Neuroreport 19, 447452.CrossRefGoogle ScholarPubMed
Fales, CL, Barch, DM, Rundle, MM, Mintun, MA, Snyder, AZ, Cohen, JD, Mathews, J, Sheline, YI (2008). Altered emotional interference processing in affective and cognitive-control brain circuitry in major depression. Biological Psychiatry 63, 377384.CrossRefGoogle ScholarPubMed
Fuster, JM (2000). Executive frontal functions. Experimental Brain Research 133, 6670.CrossRefGoogle ScholarPubMed
Gibson, B, Sanbonmatsu, DM (2004). Optimism, pessimism, and gambling: the downside of optimism. Personality and Social Psychology Bulletin 30, 149160.CrossRefGoogle ScholarPubMed
Gilbert, DT, Wilson, TD (2007). Prospection: experiencing the future. Science 317, 13511354.CrossRefGoogle ScholarPubMed
Glover, GH (1999). Deconvolution of impulse response in event-related BOLD fMRI. NeuroImage 9, 416429.CrossRefGoogle ScholarPubMed
Grimm, S, Beck, J, Schuepbach, D, Hell, D, Boesiger, P, Bermpohl, F, Niehaus, L, Boeker, H, Northoff, G (2008). 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. Biological Psychiatry 63, 369376.CrossRefGoogle ScholarPubMed
Gross, JJ, John, OP (2003). Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. Journal of Personality and Social Psychology 85, 348362.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 5662.CrossRefGoogle ScholarPubMed
Harvey, PO, Fossati, P, Pochon, JB, Levy, R, Lebastard, G, Lehericy, S, Allilaire, JF, Dubois, B (2005). Cognitive control and brain resources in major depression: an fMRI study using the n-back task. NeuroImage 26, 860869.CrossRefGoogle ScholarPubMed
Heimer, L, Van Hoesen, GW (2006). The limbic lobe and its output channels: implications for emotional functions and adaptive behaviour. Neuroscience and Biobehavioral Reviews 30, 126147.CrossRefGoogle Scholar
Herwig, U, Baumgartner, T, Kaffenberger, T, Bruhl, A, Kottlow, M, Schreiter-Gasser, U, Abler, B, Jancke, L, Rufer, M (2007 a). Modulation of anticipatory emotion and perception processing by cognitive control. NeuroImage 37, 652662.CrossRefGoogle ScholarPubMed
Herwig, U, Kaffenberger, T, Baumgartner, T, Jancke, L (2007 b). Neural correlates of a ‘pessimistic’ attitude when anticipating events of unknown emotional valence. NeuroImage 34, 848858.CrossRefGoogle ScholarPubMed
Horn, KM, Pong, M, Batni, SR, Levy, SM, Gibson, AR (2002). Functional specialization within the cat red nucleus. Journal of Neurophysiology 87, 469477.CrossRefGoogle ScholarPubMed
Johnstone, T, van Reekum, CM, Urry, HL, Kalin, NH, Davidson, RJ (2007). Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience 27, 88778884.CrossRefGoogle ScholarPubMed
Keedwell, PA, Andrew, C, Williams, SC, Brammer, MJ, Phillips, ML (2005). The neural correlates of anhedonia in major depressive disorder. Biological Psychiatry 58, 843853.CrossRefGoogle ScholarPubMed
Knutson, B, Bhanji, JP, Cooney, RE, Atlas, LY, Gotlib, IH (2008). Neural responses to monetary incentives in major depression. Biological Psychiatry 63, 686692.CrossRefGoogle ScholarPubMed
Lang, PJ (1995). The emotion probe. Studies of motivation and attention. American Psychologist 50, 372385.CrossRefGoogle ScholarPubMed
Langenecker, SA, Kennedy, SE, Guidotti, LM, Briceno, EM, Own, LS, Hooven, T, Young, EA, Akil, H, Noll, DC, Zubieta, JK (2007). Frontal and limbic activation during inhibitory control predicts treatment response in major depressive disorder. Biological Psychiatry 62, 12721280.CrossRefGoogle ScholarPubMed
Lavender, A, Watkins, E (2004). Rumination and future thinking in depression. British Journal of Clinical Psychology 43, 129142.CrossRefGoogle ScholarPubMed
Lee, BT, Seong Whi, C, Hyung Soo, K, Lee, BC, Choi, IG, Lyoo, IK, Ham, BJ (2007). The neural substrates of affective processing toward positive and negative affective pictures in patients with major depressive disorder. Progress in Neuropsychopharmacology and Biological Psychiatry 31, 14871492.CrossRefGoogle ScholarPubMed
Leppanen, JM (2006). Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Current Opinions in Psychiatry 19, 3439.CrossRefGoogle ScholarPubMed
Mayberg, HS (2003). Positron emission tomography imaging in depression: a neural systems perspective. Neuroimaging Clinics of North America 13, 805815.CrossRefGoogle ScholarPubMed
McClure, SM, York, MK, Montague, PR (2004). The neural substrates of reward processing in humans: the modern role of fMRI. Neuroscientist 10, 260268.CrossRefGoogle ScholarPubMed
Mitterschiffthaler, MT, Williams, SC, Walsh, ND, Cleare, AJ, Donaldson, C, Scott, J, Fu, CH (2008). Neural basis of the emotional Stroop interference effect in major depression. Psychological Medicine 38, 247256.CrossRefGoogle ScholarPubMed
Montgomery, SA, Åsberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382389.CrossRefGoogle ScholarPubMed
Nesse, RM (2000). Is depression an adaptation? Archives of General Psychiatry 57, 1420.CrossRefGoogle ScholarPubMed
Nichols, T, Brett, M, Andersson, J, Wager, T, Poline, JB (2005). Valid conjunction inference with the minimum statistic. NeuroImage 25, 653660.CrossRefGoogle ScholarPubMed
Nitschke, JB, Sarinopoulos, I, Mackiewicz, KL, Schaefer, HS, Davidson, RJ (2006). Functional neuroanatomy of aversion and its anticipation. NeuroImage 29, 106116.CrossRefGoogle ScholarPubMed
Norem, JK, Cantor, N (1986). Defensive pessimism: harnessing anxiety as motivation. Journal of Personality and Social Psychology 51, 12081217.CrossRefGoogle ScholarPubMed
Northoff, G, Bermpohl, F (2004). Cortical midline structures and the self. Trends in Cognitive Sciences 8, 102107.CrossRefGoogle ScholarPubMed
Panksepp, J (2006). Emotional endophenotypes in evolutionary psychiatry. Progress in Neuropsychopharmacology and Biological Psychiatry 30, 774784.CrossRefGoogle ScholarPubMed
Paulus, MP, Feinstein, JS, Castillo, G, Simmons, AN, Stein, MB (2005). Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. Archives of General Psychiatry 62, 282288.CrossRefGoogle ScholarPubMed
Paulus, MP, Stein, MB (2006). An insular view of anxiety. Biological Psychiatry 60, 383387.CrossRefGoogle ScholarPubMed
Pessoa, L (2008). On the relationship between emotion and cognition. Nature Reviews Neuroscience 9, 148158.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biological Psychiatry 54, 515528.CrossRefGoogle ScholarPubMed
Pyszczynski, T, Holt, K, Greenberg, J (1987). Depression, self-focused attention, and expectancies for positive and negative future life events for self and others. Journal of Personality and Social Psychology 52, 994–1001.CrossRefGoogle ScholarPubMed
Sharot, T, Riccardi, AM, Raio, CM, Phelps, EA (2007). Neural mechanisms mediating optimism bias. Nature 450, 102105.CrossRefGoogle ScholarPubMed
Shepperd, JA, McNulty, JK (2002). The affective consequences of expected and unexpected outcomes. Psychological Science 13, 8588.CrossRefGoogle ScholarPubMed
Siegle, GJ, Thompson, W, Carter, CS, Steinhauer, SR, Thase, ME (2007). Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biological Psychiatry 61, 198209.CrossRefGoogle ScholarPubMed
Simmons, A, Matthews, SC, Paulus, MP, Stein, MB (2008). Intolerance of uncertainty correlates with insula activation during affective ambiguity. Neuroscience Letters 430, 9297.CrossRefGoogle ScholarPubMed
Soares, JC, Mann, JJ (1997). The anatomy of mood disorders – review of structural neuroimaging studies. Biological Psychiatry 41, 86–106.CrossRefGoogle ScholarPubMed
Sporns, O, Honey, CJ, Kotter, R (2007). Identification and classification of hubs in brain networks. PLoS ONE 2, e1049.CrossRefGoogle ScholarPubMed
Talairach, J, Tournoux, P (1988). Co-planar Stereotaxic Atlas of the Human Brain. Thieme: Stuttgart.Google Scholar
Vogt, BA (2005). Pain and emotion interactions in subregions of the cingulate gyrus. Nature Reviews Neuroscience 6, 533544.CrossRefGoogle ScholarPubMed
Yamasaki, H, LaBar, KS, McCarthy, G (2002). Dissociable prefrontal brain systems for attention and emotion. Proceedings of the National Academy of Sciences of the USA 99, 1144711451.CrossRefGoogle ScholarPubMed
Yuste, R, MacLean, JN, Smith, J, Lansner, A (2005). The cortex as a central pattern generator. Nature Reviews Neuroscience 6, 477483.CrossRefGoogle ScholarPubMed
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