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Drug-free patients with major depression show an increased electrophysiological response to valid and invalid feedback

Published online by Cambridge University Press:  13 May 2011

G. W. Mies
Affiliation:
Department of Psychiatry, Erasmus MC, University Medical Center Rotterdam, The Netherlands
F. M. van der Veen*
Affiliation:
Department of Psychiatry, Erasmus MC, University Medical Center Rotterdam, The Netherlands
J. H. M. Tulen
Affiliation:
Department of Psychiatry, Erasmus MC, University Medical Center Rotterdam, The Netherlands
T. K. Birkenhäger
Affiliation:
Department of Psychiatry, Erasmus MC, University Medical Center Rotterdam, The Netherlands
M. W. Hengeveld
Affiliation:
Department of Psychiatry, Erasmus MC, University Medical Center Rotterdam, The Netherlands
M. W. van der Molen
Affiliation:
Department of Psychology, University of Amsterdam, The Netherlands
*
*Address for correspondence: Dr F. M. van der Veen, Department of Psychiatry, Erasmus MC, PO Box 2040, 3000 CA Rotterdam, The Netherlands. (Email: f.vanderveen@erasmusmc.nl)

Abstract

Background

Depressed patients are biased in their response to negative information. They have been found to show a maladaptive behavioral and aberrant electrophysiological response to negative feedback. The aim of this study was to investigate the behavioral and electrophysiological response to feedback validity in drug-free depressed patients.

Method

Fifteen drug-free in-patients with unipolar major depression disorder (MDD) and 30 demographically matched controls performed a time-estimation task in which they received valid and invalid (i.e. related and unrelated to performance) positive and negative feedback. The number of behavioral adjustments to the feedback and the feedback-related negativity (FRN) were measured.

Results

Patients made fewer correct adjustments after valid negative feedback than controls, and their FRNs were larger. Neither patients nor controls adjusted their time estimates following invalid negative feedback.

Conclusions

The FRN results suggest that depressed drug-free in-patients have an atypical rostral anterior cingulate response to feedback that is independent of feedback validity. Their behavioral response to invalid negative feedback, however, is not impaired. This study confirms the notion that the behavioral responses of depressed individuals to negative feedback are context dependent.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2011

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References

Beats, BC, Sahakian, BJ, Levy, R (1996). Cognitive performance in tests sensitive to frontal lobe dysfunction in the elderly depressed. Psychological Medicine 26, 591603.Google Scholar
Beck, AT (1979). Cognitive Theory of Depression. John Wiley and Sons: New York.Google Scholar
Bush, G, Luu, P, Posner, MI (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215222.Google Scholar
Chiu, PH, Deldin, PJ (2007). Neural evidence for enhanced error detection in major depressive disorder. American Journal of Psychiatry 164, 608616.Google Scholar
Cohen, J (1988). Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates: Hillsdale, NJ.Google Scholar
Compton, RJ, Lin, M, Vargas, G, Carp, J, Fineman, SL, Quandt, LC (2008). Error detection and posterror behavior in depressed undergraduates. Emotion 8, 5867.Google Scholar
Davidson, RJ, Pizzagalli, D, Nitschke, JB, Putnam, K (2002). Depression: perspectives from affective neuroscience. Annual Review of Psychology 53, 545574.Google Scholar
De Bruijn, ER, Hulstijn, W, Verkes, RJ, Ruigt, GS, Sabbe, BG (2004). Drug-induced stimulation and suppression of action monitoring in healthy volunteers. Psychopharmacology (Berlin) 177, 151160.Google Scholar
De Bruijn, ER, Sabbe, BG, Hulstijn, W, Ruigt, GS, Verkes, RJ (2006). Effects of antipsychotic and antidepressant drugs on action monitoring in healthy volunteers. Brain Research 1105, 122129.Google Scholar
Douglas, KM, Porter, RJ, Frampton, CM, Gallagher, P, Young, AH (2009). Abnormal response to failure in unmedicated major depression. Journal of Affective Disorders 119, 9299.Google Scholar
Ekman, P, Friesen, WV (1978). Facial Action Coding System: A Technique for the Measurement of Facial Movement. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Elliott, R, Sahakian, BJ, Herrod, JJ, Robbins, TW, Paykel, ES (1997). Abnormal response to negative feedback in unipolar depression: evidence for a diagnosis specific impairment. Journal of Neurology, Neurosurgery and Psychiatry 63, 7482.Google Scholar
Elliott, R, Sahakian, BJ, McKay, AP, Herrod, JJ, Robbins, TW, Paykel, ES (1996). Neuropsychological impairments in unipolar depression: the influence of perceived failure on subsequent performance. Psychological Medicine 26, 975989.Google Scholar
Eppinger, B, Kray, J, Mock, B, Mecklinger, A (2008). Better or worse than expected? Aging, learning, and the ERN. Neuropsychologia 46, 521539.Google Scholar
Eshel, N, Roiser, JP (2010). Reward and punishment processing in depression. Biological Psychiatry 68, 118124.Google Scholar
Evers, EA, Cools, R, Clark, L, van der Veen, FM, Jolles, J, Sahakian, BJ, Robbins, TW (2005). Serotonergic modulation of prefrontal cortex during negative feedback in probabilistic reversal learning. Neuropsychopharmacology 30, 11381147.Google Scholar
Fallgatter, AJ, Herrmann, MJ, Roemmler, J, Ehlis, AC, Wagener, A, Heidrich, A, Ortega, G, Zeng, Y, Lesch, KP (2004). Allelic variation of serotonin transporter function modulates the brain electrical response for error processing. Neuropsychopharmacology 29, 15061511.Google Scholar
Fladung, AK, Baron, U, Gunst, I, Kiefer, M (2010). Cognitive reappraisal modulates performance following negative feedback in patients with major depressive disorder. Psychological Medicine 40, 17031710.Google Scholar
Foti, D, Weinberg, A, Dien, J, Hajcak, G (2010). Parsing event-related potentials to rewards and non-rewards using temporal-spatial PCA: the feedback negativity is the absence of a reward-related positivity. SPR 50th Annual Meeting, Portland, OR, USA.Google Scholar
Gehring, WJ, Himle, J, Nisenson, LG (2000). Action-monitoring dysfunction in obsessive-compulsive disorder. Psychological Science 11, 16.Google Scholar
Gratton, G, Coles, MG, Donchin, E (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology 55, 468484.Google Scholar
Hajcak, G, McDonald, N, Simons, RF (2003). Anxiety and error-related brain activity. Biological Psychology 64, 7790.Google Scholar
Hajcak, G, McDonald, N, Simons, RF (2004). Error-related psychophysiology and negative affect. Brain and Cognition 56, 189197.Google Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 5662.Google Scholar
Holmes, AJ, Pizzagalli, DA (2008). Spatiotemporal dynamics of error processing dysfunctions in major depressive disorder. Archives of General Psychiatry 65, 179188.Google Scholar
Holmes, AJ, Pizzagalli, DA (2010). Effects of task-relevant incentives on the electrophysiological correlates of error processing in major depressive disorder. Cognitive, Affective and Behavioral Neuroscience 10, 119128.Google Scholar
Jocham, G, Ullsperger, M (2009). Neuropharmacology of performance monitoring. Neuroscience and Biobehavioral Reviews 33, 4860.Google Scholar
Johannes, S, Wieringa, BM, Nager, W, Dengler, R, Munte, TF (2001 a). Oxazepam alters action monitoring. Psychopharmacology (Berlin) 155, 100106.Google Scholar
Johannes, S, Wieringa, BM, Nager, W, Rada, D, Dengler, R, Emrich, HM, Munte, TF, Dietrich, DE (2001 b). Discrepant target detection and action monitoring in obsessive-compulsive disorder. Psychiatry Research 108, 101110.Google Scholar
Koolschijn, PC, van Haren, NE, Lensvelt-Mulders, GJ, Hulshoff Pol, HE, Kahn, RS (2009). Brain volume abnormalities in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Human Brain Mapping 30, 37193735.Google Scholar
Luu, P, Collins, P, Tucker, DM (2000). Mood, personality, and self-monitoring: negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. Journal of Experimental Psychology: General 129, 4360.Google Scholar
Mathewson, KJ, Dywan, J, Snyder, PJ, Tays, WJ, Segalowitz, SJ (2008). Aging and electrocortical response to error feedback during a spatial learning task. Psychophysiology 45, 936948.Google Scholar
Mayberg, HS (1997). Limbic-cortical dysregulation: a proposed model of depression. Journal of Neuropsychiatry and Clinical Neurosciences 9, 471481.Google Scholar
Mayberg, HS (2003). Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. British Medical Bulletin 65, 193207.Google Scholar
Mies, GW, van der Molen, MW, Smits, M, Hengeveld, MW, van der Veen, FM (2011). The anterior cingulate cortex responds differently to the validity and valence of feedback in a time-estimation task. NeuroImage. Published online: 13 April 2011. doi:10.1016/j.neuroimage.2011.04.015.Google Scholar
Mies, GW, van der Veen, FM, Tulen, JHM, Hengeveld, MW, van der Molen, MW (in press). Cardiac and electrophysiological responses to valid and invalid feedback in a time-estimation task. Journal of Psychophysiology.Google Scholar
Miltner, WHR, Braun, CH, Coles, MGH (1997). Event-related brain potentials following incorrect feedback in a time-estimation task: evidence for a ‘generic’ neural system for error detection. Journal of Cognitive Neuroscience 9, 788798.Google Scholar
Murphy, FC, Michael, A, Robbins, TW, Sahakian, BJ (2003). Neuropsychological impairment in patients with major depressive disorder: the effects of feedback on task performance. Psychological Medicine 33, 455467.Google Scholar
Nieuwenhuis, S, Slagter, HA, von Geusau, NJ, Heslenfeld, DJ, Holroyd, CB (2005). Knowing good from bad: differential activation of human cortical areas by positive and negative outcomes. European Journal of Neuroscience 21, 31613168.Google Scholar
Olvet, DM, Klein, DN, Hajcak, G (2010). Depression symptom severity and error-related brain activity. Psychiatry Research 179, 3037.Google Scholar
Pizzagalli, DA (2011). Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 36, 183206.Google Scholar
Riba, J, Rodriguez-Fornells, A, Morte, A, Munte, TF, Barbanoj, MJ (2005). Noradrenergic stimulation enhances human action monitoring. Journal of Neuroscience 25, 43704374.Google Scholar
Ridderinkhof, KR, Ullsperger, M, Crone, EA, Nieuwenhuis, S (2004). The role of the medial frontal cortex in cognitive control. Science 306, 443447.Google Scholar
Ruchsow, M, Herrnberger, B, Beschoner, P, Gron, G, Spitzer, M, Kiefer, M (2006). Error processing in major depressive disorder: evidence from event-related potentials. Journal of Psychiatric Research 40, 3746.Google Scholar
Ruchsow, M, Herrnberger, B, Wiesend, C, Gron, G, Spitzer, M, Kiefer, M (2004). The effect of erroneous responses on response monitoring in patients with major depressive disorder: a study with event-related potentials. Psychophysiology 41, 833840.Google Scholar
Santesso, DL, Steele, KT, Bogdan, R, Holmes, AJ, Deveney, CM, Meites, TM, Pizzagalli, DA (2008). Enhanced negative feedback responses in remitted depression. Neuroreport 19, 10451048.Google Scholar
Schrijvers, D, de Bruijn, ER, Maas, Y, De Grave, C, Sabbe, BG, Hulstijn, W (2008). Action monitoring in major depressive disorder with psychomotor retardation. Cortex 44, 569579.Google Scholar
Schrijvers, D, De Bruijn, ER, Maas, YJ, Vancoillie, P, Hulstijn, W, Sabbe, BG (2009). Action monitoring and depressive symptom reduction in major depressive disorder. International Journal of Psychophysiology 71, 218224.Google Scholar
Sharbrough, F, Chatrian, G-E, Lesser, RP, Luders, H, Nuwer, M, Picton, TW (1991). American Electroencephalographic Society guidelines for standard electrode position nomenclature. Journal of Clinical Neurophysiology 8, 200202.Google Scholar
Steele, JD, Kumar, P, Ebmeier, KP (2007). Blunted response to feedback information in depressive illness. Brain 130, 23672374.Google Scholar
Steffens, DC, Wagner, HR, Levy, RM, Horn, KA, Krishnan, KR (2001). Performance feedback deficit in geriatric depression. Biological Psychiatry 50, 358363.Google Scholar
Stern, ER, Liu, Y, Gehring, WJ, Lister, JJ, Yin, G, Zhang, J, Fitzgerald, KD, Himle, JA, Abelson, JL, Taylor, SF (2010). Chronic medication does not affect hyperactive error responses in obsessive-compulsive disorder. Psychophysiology 47, 913920.Google Scholar
Taylor Tavares, JV, Clark, L, Furey, ML, Williams, GB, Sahakian, BJ, Drevets, WC (2008). Neural basis of abnormal response to negative feedback in unmedicated mood disorders. NeuroImage 42, 11181126.Google Scholar
Tucker, DM, Luu, P, Frishkoff, G, Quiring, J, Poulsen, C (2003). Frontolimbic response to negative feedback in clinical depression. Journal of Abnormal Psychology 112, 667678.Google Scholar
van den Bosch, RJ, Rombouts, RP, van Asma, MJ (1996). What determines Continuous Performance Task performance? Schizophrenia Bulletin 22, 643651.Google Scholar
van der Elst, W, van Boxtel, MP, van Breukelen, GJ, Jolles, J (2008). A large-scale cross-sectional and longitudinal study into the ecological validity of neuropsychological test measures in neurologically intact people. Archives of Clinical Neuropsychology 23, 787800.Google Scholar
van der Veen, F, Evers, E, Mies, G, Vuurman, E, Jolles, J (2009). Acute tryptophan depletion selectively attenuates cardiac slowing in an Eriksen flanker task. Journal of Psychopharmacology 24, 14551463.Google Scholar
van der Veen, FM, Mies, GW, van der Molen, MW, Evers, EA (2008). Acute tryptophan depletion in healthy males attenuates phasic cardiac slowing but does not affect electro-cortical response to negative feedback. Psychopharmacology (Berlin) 199, 255263.Google Scholar
van der Veen, FM, Roder, CH, Mies, GW, van der Lugt, A, Smits, M (2011). Remedial action and feedback processing in a time-estimation task: evidence for a role of the rostral cingulate zone in behavioral adjustments without learning. NeuroImage 54, 447454.Google Scholar
van Tol, MJ, van der Wee, NJ, van den Heuvel, OA, Nielen, MM, Demenescu, LR, Aleman, A, Renken, R, van Buchem, MA, Zitman, FG, Veltman, DJ (2010). Regional brain volume in depression and anxiety disorders. Archives of General Psychiatry 67, 10021011.Google Scholar
Wechsler, D (1997). Wechsler Adult Intelligence Scale-III (WAIS-III). Psychological Corporation: San Antonio, TX.Google Scholar
Wild-Wall, N, Willemssen, R, Falkenstein, M (2009). Feedback-related processes during a time-production task in young and older adults. Clinical Neurophysiology 120, 407413.Google Scholar
Wu, Y, Zhou, X (2009). The P300 and reward valence, magnitude, and expectancy in outcome evaluation. Brain Research 1286, 114122.Google Scholar