Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-25T18:16:03.116Z Has data issue: false hasContentIssue false

Prefrontal cortex function in remitted major depressive disorder

Published online by Cambridge University Press:  01 October 2012

N. L. Nixon*
Affiliation:
Division of Psychiatry, The Institute of Mental Health, University of Nottingham, Nottingham, UK
P. F. Liddle
Affiliation:
Division of Psychiatry, The Institute of Mental Health, University of Nottingham, Nottingham, UK
G. Worwood
Affiliation:
Division of Psychiatry, The Institute of Mental Health, University of Nottingham, Nottingham, UK
M. Liotti
Affiliation:
Department of Psychology, Simon Fraser University, Vancouver, Canada
E. Nixon
Affiliation:
Division of Psychiatry, The Institute of Mental Health, University of Nottingham, Nottingham, UK
*
*Address for correspondence: Dr N. L. Nixon, Division of Psychiatry, The Institute of Mental Health, University of NottinghamInnovation Park, Triumph Road, Nottingham NG7 2TU, UK. (Email: [email protected])

Abstract

Background

Recent models of major depressive disorder (MDD) have proposed the rostral anterior cingulate (rACC) and dorsomedial prefrontal cortex (dmPFC) as nexus sites in the dysfunctional regulation of cognitive-affective state. Limited evidence from remitted-state MDD supports these theories by suggesting that aberrant neural activity proximal to the rACC and the dmPFC may play a role in vulnerability to recurrence/relapse within this disorder. Here we present a targeted analysis assessing functional activity within these two regions of interest (ROIs) for groups with identified vulnerability to MDD: first, remitted, high predicted recurrence-risk patients; and second, patients suffering observed 1-year recurrence.

Method

Baseline T2* images sensitive to blood oxygen level-dependent (BOLD) contrast were acquired from patients and controls during a Go/No-Go (GNG) task incorporating negative feedback, with 1-year patient follow-up to identify recurrence. BOLD contrast data for error commission (EC) and visual negative feedback (VNF) were used in an ROI analysis based on rACC and dmPFC coordinates from the literature, comparing patients versus controls and recurrence versus non-recurrence versus control groups.

Results

Analysis of patients (n = 20) versus controls (n = 20) showed significant right dmPFC [Brodmann area (BA) 9] hypoactivity within the patient group, co-localized during EC and VNF, with additional significant rACC (BA 32) hypoactivity during EC. The results from the follow-up analysis were undermined by small groups and potential confounders but suggested persistent right dmPFC (BA 9) hypoactivity associated with 1-year recurrence.

Conclusions

Convergent hypoactive right dmPFC (BA 9) processing of VNF and EC, possibly impairing adaptive reappraisal of negative experience, was associated most clearly with clinically predicted vulnerability to MDD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abramson, LY, Metalsky, GI, Alloy, LB (1989). Hopeless depression: a theory-based subtype of depression. Psychological Review 96, 358372.CrossRefGoogle Scholar
Alexopoulos, GS, Murphy, CF, Gunning-Dixon, FM, Kalayam, B, Katz, R, Kanellopoulos, D (2007). Event-related potentials in an emotional go/no-go task and remission of geriatric depression. Neuroreport 18, 217221.CrossRefGoogle Scholar
Ammons, RB, Ammons, CH (1962). The Quick Test: Provisional manual. Psychological Reports 11, 111161.CrossRefGoogle Scholar
Anand, A, Li, Y, Wang, Y, Wu, J, Gao, S, Bukhari, L, Mathews, VP, Kalnin, A, Lowe, MJ (2005 a). Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biological Psychiatry 57, 10791088.CrossRefGoogle ScholarPubMed
Anand, A, Li, Y, Wang, Y, Wu, J, Gao, S, Bukhari, L, Mathews, VP, Kalnin, A, Lowe, MJ (2005 b). Antidepressant effect on connectivity of the mood-regulating circuit: an fMRI study. Neuropsychopharmacology 30, 13341344.CrossRefGoogle ScholarPubMed
Beck, AT (1987). Cognitive models of depression. Journal of Cognitive Psychotherapy 1, 537.Google Scholar
Beck, AT, Steer, RA, Ball, R, Ranieri, WF (1996). Comparison of Beck Depression Inventories-IA and -II in psychiatric outpatients. Journal of Personality Assessment 67, 588597.CrossRefGoogle Scholar
Bremner, J, Innis, RB, Salomon, RM, Staib, LH, Ng, CK, Miller, HL, Bronen, RA, Krystal, JH, Duncan, J, Dayton, R, Lawrence, H, Malison, R, Holley, D, Soufer, R, Charney, DS (1997). Positron emission tomography measurement of cerebral metabolic correlates of tryptophan depletion-induced depressive relapse. Archives of General Psychiatry 54, 364374.CrossRefGoogle ScholarPubMed
Bremner, J, Vythilingam, M, Ng, CK, Vermetten, E (2003). Regional brain metabolic correlates of {alpha}-methylparatyrosine-induced depressive symptoms: implications for the neural circuitry of depression. Journal of the American Medical Association 289, 31253134.CrossRefGoogle ScholarPubMed
Brett, M, Anton, J-L, Valabregue, R, Poline, J-B (2002). Region of interest analysis using an SPM toolbox [abstract]. NeuroImage 16, abstract 497.Google Scholar
Brett, M, Christoff, K, Cusack, R, Lancaster, J (2001). Using the Talairach atlas with the MNI template. NeuroImage 13, S85.CrossRefGoogle Scholar
Buchsbaum, MS, Wu, J, Siegel, BV, Hackett, E, Trenary, M, Lennert, A, Reynolds, C (1997). Effect of sertraline on regional metabolic rate in patients with affective disorder. Biological Psychiatry 41, 1522.CrossRefGoogle ScholarPubMed
Chiu, PH, Deldin, PJ (2007). Neural evidence for enhanced error detection in major depressive disorder. American Journal of Psychiatry 164, 608616.CrossRefGoogle ScholarPubMed
Davidson, RJ, Irwin, W (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Sciences 3, 1121.CrossRefGoogle ScholarPubMed
Davidson, RJ, Pizzagalli, D, Nitschke, JB, Putnam, K (2002). Depression: perspectives from affective neuroscience. Annual Review of Psychology 53, 545574.CrossRefGoogle ScholarPubMed
Delaveau, P, Jabourian, M, Lemogne, C, Guionnet, S, Bergouignan, L, Fossati, P (2011). Brain effects of antidepressants in major depression: a meta-analysis of emotional processing studies. Journal of Affective Disorders 130, 6674.CrossRefGoogle ScholarPubMed
Drevets, WC, Price, JL, Furey, ML (2008). Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Structure and Function 213, 93118.CrossRefGoogle ScholarPubMed
Eysenck, HJ, Eysenck, SBG (1991). Manual of the Eysenck Personality Scales. Hodder & Stoughton: London.Google Scholar
Falkenstein, M, Hoormann, J, Christ, S, Hohnsbein, J (2000). ERP components on reaction errors and their functional significance: a tutorial. Biological Psychology 51, 87107.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1997). Structured Clinical Interview for DSM-IV Axis I Disorders – Clinician Version (SCID-CV). American Psychiatric Press: Washington, DC.Google Scholar
Fitzgerald, PB, Oxley, TJ, Laird, AR, Kulkarni, J, Egan, GF, Daskalakis, ZJ (2006). An analysis of functional neuroimaging studies of dorsolateral prefrontal cortical activity in depression. Psychiatry Research 148, 3345.CrossRefGoogle ScholarPubMed
Folstein, MF, Folstein, SE, McHugh, PR (1975). ‘Mini-mental state’. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 12, 189198.CrossRefGoogle Scholar
Geddes, JR, Carney, SM, Davies, C, Furukawa, TA, Kupfer, DJ, Frank, E, Goodwin, GM (2003). Relapse prevention with antidepressant drug treatment in depressive disorders: a systematic review. Lancet 361, 653661.CrossRefGoogle ScholarPubMed
Gehring, WJ, Goss, WJ, Coles, MGH, Meyer, DE, Donchin, E (1993). A neural system for error detection and compensation. Psychological Science 4, 385389.CrossRefGoogle Scholar
Georgiadi, E, Liotti, M, Nixon, NL, Liddle, PF (2011). Electrophysiological evidence for abnormal error monitoring in recurrent major depressive disorder. Psychophysiology 48, 111.CrossRefGoogle ScholarPubMed
Goldin, PR, McRae, K, Ramel, W, Gross, JJ (2008). The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biological Psychiatry 63, 577586.CrossRefGoogle ScholarPubMed
Greicius, MD, Flores, BH, Menon, V, Glover, GH, Solvason, HB, Kenna, H, Reiss, AL, Schatzberg, AF (2007). Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biological Psychiatry 62, 429437.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 5662.CrossRefGoogle ScholarPubMed
Harvey, P-O, Fossati, P, Pochon, J-B, Levy, R, Lebastard, G, Lehéricy, S, Allilaire, J-F, Dubois, B (2005). Cognitive control and brain resources in major depression: an fMRI study using the n-back task. NeuroImage 26, 860869.CrossRefGoogle ScholarPubMed
Holmes, AJ, Pizzagalli, DA (2007). Task feedback effects on conflict monitoring and executive control: relationship to subclinical measures of depression. Emotion 7, 6876.CrossRefGoogle ScholarPubMed
Holmes, AJ, Pizzagalli, DA (2008). Spatio-temporal dynamics of error processing dysfunctions in major depressive disorder. Archives of General Psychiatry 65, 179188.CrossRefGoogle Scholar
Hyler, SE (1994). Personality Diagnostic Questionnaire (PDQ-4+). New York State Psychiatric Institute: New York.Google Scholar
Johansen-Berg, H, Gutman, DA, Behrens, TEJ, Matthews, PM, Rushworth, MFS, Katz, E, Lozano, AM, Mayberg, HS (2008). Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cerebral Cortex 18, 13741383.CrossRefGoogle ScholarPubMed
Judd, LL (1997). The clinical course of unipolar major depressive disorders. Archives of General Psychiatry 54, 989991.CrossRefGoogle ScholarPubMed
Kelley, WM, Macrae, CN, Wyland, CL, Caglar, S, Inati, S, Heatherton, TF (2002). Finding the self? An event-related fMRI study. Journal of Cognitive Neuroscience 145, 785794.CrossRefGoogle Scholar
Kennedy, N, Paykel, ES (2004). Residual symptoms at remission from depression: impact on long-term outcome. Journal of Affective Disorders 80, 135144.CrossRefGoogle ScholarPubMed
Kennedy, SH, Evans, KR, Krüger, S, Mayberg, HS, Meyer, JH, McCann, S, Arifuzzman, AI, Houle, S, Vaccarino, FJ (2001). Changes in regional brain glucose metabolism measured with positron emission tomography after paroxetine treatment of major depression. American Journal of Psychiatry 158, 899905.CrossRefGoogle ScholarPubMed
Kiehl, KA, Liddle, PF, Hopfinger, JB (2000). Error processing and the rostral anterior cingulate: an event-related fMRI study. Psychophysiology 37, 216223.CrossRefGoogle ScholarPubMed
Laming, DRJ (1968). Information Theory of Choice-Reaction Times. Academic Press: London.Google Scholar
Laurens, KR, Ngan, ETC, Bates, AT, Kiehl, KA, Liddle, PF (2003). Rostral anterior cingulate cortex dysfunction during error processing in schizophrenia. Brain 126, 610622.CrossRefGoogle ScholarPubMed
Lemogne, C, le Bastard, G, Mayberg, H, Volle, E, Bergouignan, L, Lehéricy, S, Allilaire, J-F, Fossati, P (2009). In search of the depressive self: extended medial prefrontal network during self-referential processing in major depression. Social Cognitive and Affective Neuroscience 4, 305312.CrossRefGoogle ScholarPubMed
Liotti, M, Mayberg, H, McGinnis, S, Brannan, S, Jerabek, P (2002). Unmasking disease-specific cerebral blood flow abnormalities: mood challenge in patients with remitted unipolar depression. American Journal of Psychiatry 159, 18301840.CrossRefGoogle ScholarPubMed
Maj, M, Veltro, F, Pirozzi, R, Lobrace, S, Magliano, L (1992). Pattern of recurrence of illness after recovery from an episode of major depression: a prospective study. American Journal of Psychiatry 149, 795800.Google ScholarPubMed
Marsh, AA, Blair, KS, Vythilingam, M, Busis, S, Blair, R (2007). Response options and expectations of reward in decision-making: the differential roles of dorsal and rostral anterior cingulate cortex. NeuroImage 35, 979988.CrossRefGoogle ScholarPubMed
Mayberg, HS (1997). Limbic-cortical dysregulation: a proposed model of depression. Journal of Neuropsychiatry and Clinical Neurosciences 9, 471481.Google ScholarPubMed
Mayberg, HS (2003). Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimized treatment. British Medical Bulletin 65, 193207.CrossRefGoogle Scholar
Mayberg, HS (2007). Defining the neural circuitry of depression: toward a new nosology with therapeutic implications. Biological Psychiatry 61, 729730.CrossRefGoogle Scholar
Mayberg, HS, Brannan, S, Mahurin, RK, Jerabek, PA, Brickman, JS, Tekell, JL, Arturo Silva, J, McGinnis, S, Glass, TG, Martin, CC, Fox, PT (1997). Cingulate function in depression: a potential predictor of treatment response. Neuroreport 8, 10571061.CrossRefGoogle ScholarPubMed
Neumeister, A, Nugent, A, Waldeck, T, Geraci, M, Schwarz, M, Bonne, O, Bain, EE, Luckenbaugh, DA, Herscovitch, P, Charney, DS, Drevets, WC (2004). Neural and behavioral responses to tryptophan depletion in unmedicated patients with remitted major depressive disorder and controls. Archives of General Psychiatry 61, 765773.CrossRefGoogle ScholarPubMed
Nierenberg, AA, Husain, MM, Trivedi, MH, Fava, M, Warden, D, Wisniewski, SR, Miyahara, S, Rush, AJ (2010). Residual symptoms after remission of major depressive disorder with citalopram and risk of relapse: a STAR*D report. Psychological Medicine 40, 4150.CrossRefGoogle ScholarPubMed
Norbury, R, Selvaraj, S, Taylor, MJ, Harmer, C, Cowen, PJ (2010). Increased neural response to fear in patients recovered from depression: a 3T functional magnetic resonance imaging study. Psychological Medicine 40, 425432.CrossRefGoogle ScholarPubMed
Ochsner, KN, Gross, JJ (2005). The cognitive control of emotion. Trends in Cognitive Sciences 9, 242249.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97113.CrossRefGoogle ScholarPubMed
Pailing, PE, Segalowitz, SJ, Dywan, J, Davies, PL (2002). Error negativity and response control. Psychophysiology 39, 198206.CrossRefGoogle ScholarPubMed
Pizzagalli, D, Pascual-Marqui, R, Nitschke, J, Oakes, T, Larson, C, Abercrombie, HC, Schaefer, SM, Koger, JV, Benca, R, Davidson, RJ (2001). Anterior cingulate activity as a predictor of degree of treatment response in major depression: evidence from brain electrical tomography analysis. American Journal of Psychiatry 158, 405415.CrossRefGoogle ScholarPubMed
Polli, FE, Barton, JJS, Thakkar, KN, Greve, DN, Goff, DC, Rauch, SL, Manoach, DS (2008). Reduced error-related activation in two anterior cingulate circuits is related to impaired performance in schizophrenia. Brain 131, 971986.CrossRefGoogle ScholarPubMed
Ramana, R, Paykel, ES, Cooper, Z, Hayhurst, H, Saxty, M, Surtees, PG (1995). Remission and relapse in major depression: a two-year prospective follow-up study. Psychological Medicine 25, 11611170.CrossRefGoogle ScholarPubMed
Ridderinkhof, KR, Ullsperger, M, Crone, EA, Nieuwenhuis, S (2004). The role of the medial frontal cortex in cognitive control. Science 306, 443447.CrossRefGoogle ScholarPubMed
Ruchsow, M, Herrnberger, B, Beschoner, P, Grön, G, Spitzer, M, Keifer, M (2006). Error processing in major depressive disorder: evidence from event-related potentials. Journal of Psychiatric Research 40, 3746.CrossRefGoogle ScholarPubMed
Seminowicz, D, Mayberg, HS, McIntosh, A, Goldapple, K, Kennedy, S, Segal, Z, Rafi-Tari, S (2004). Limbic-frontal circuitry in major depression: a path modeling meta analysis. NeuroImage 22, 409418.CrossRefGoogle Scholar
Sheline, YI, Price, JL, Yan, Z, Mintun, MA (2010). Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proceedings of the National Academy of Sciences USA 107, 1102011025.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
Vanderhasselt, MA, De Raedt, R (2009). Impairments in cognitive control persist during remission from depression and are related to the number of past episodes: an event related potentials study. Biological Psychology 81, 169176.CrossRefGoogle Scholar
Williams, N, Simpson, AN, Simpson, K, Nahas, Z (2009). Relapse rates with long-term antidepressant drug therapy: a meta-analysis. Human Psychopharmacology 24, 401408.CrossRefGoogle ScholarPubMed
Wu, J, Buchsbaum, MS, Gillin, JC, Tang, C, Cadwell, S, Wiegand, M, Najafi, A, Klein, E, Hazen, K, Bunney, WE (1999). Prediction of antidepressant effects of sleep deprivation by metabolic rates in the ventral anterior cingulate and medial prefrontal cortex. American Journal of Psychiatry 156, 11491158.CrossRefGoogle ScholarPubMed
Zhou, Y, Yu, C, Zheng, H, Liu, Y, Song, M, Qin, W, Li, K, Jiang, T (2010). Increased neural resources recruitment in the intrinsic organization in major depression. Journal of Affective Disorders 121, 220230.CrossRefGoogle ScholarPubMed
Supplementary material: File

Nixon supplementary material 1

Nixon supplementary material 1

Download Nixon supplementary material 1(File)
File 52.7 KB
Supplementary material: File

Nixon supplementary material 2

Nixon supplementary material 2

Download Nixon supplementary material 2(File)
File 26.1 KB
Supplementary material: File

Nixon supplementary material 3

Nixon supplementary material 3

Download Nixon supplementary material 3(File)
File 38.4 KB
Supplementary material: File

Nixon supplementary material 4

Nixon supplementary material 4

Download Nixon supplementary material 4(File)
File 73.2 KB
Supplementary material: File

Nixon supplementary material 5

Nixon supplementary material 5

Download Nixon supplementary material 5(File)
File 51.7 KB