Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T17:06:40.460Z Has data issue: false hasContentIssue false
  • English
  • Français

Cognitive inhibition in depression and suicidal behavior: a neuroimaging study

Published online by Cambridge University Press:  16 December 2015

S. Richard-Devantoy ,
Y. Ding ,
M. Lepage ,
G. Turecki  and
F. Jollant
S. Richard-Devantoy
Affiliation:
Department of Psychiatry & Douglas Mental Health University Institute, McGill Group for Suicide Studies, McGill University, Montréal, Québec, Canada Hôpital de Saint-Jérôme, Saint-Jérôme (Qc), Canada and Laboratoire de Psychologie des Pays de la Loire, UPRES EA 4638, Université d'Angers, Angers, France
Y. Ding
Affiliation:
Department of Psychiatry & Douglas Mental Health University Institute, McGill Group for Suicide Studies, McGill University, Montréal, Québec, Canada
M. Lepage
Affiliation:
Department of Psychiatry & Douglas Mental Health University Institute, McGill University, Montréal, Québec, Canada
G. Turecki
Affiliation:
Department of Psychiatry & Douglas Mental Health University Institute, McGill Group for Suicide Studies, McGill University, Montréal, Québec, Canada
F. Jollant*
Affiliation:
Department of Psychiatry & Douglas Mental Health University Institute, McGill Group for Suicide Studies, McGill University, Montréal, Québec, Canada Department of Psychiatry, CHU Nîmes, France
*
*Address for correspondence: F. Jollant, Douglas Mental Health University Institute, Frank B. Common Building, 6875 LaSalle Boulevard, Montréal, Québec, H4H 1R3, Canada. (Email: fabrice.jollant@mcgill.ca)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Cognitive inhibition deficits have previously been found in suicide attempters. This study examined the neural basis for these deficits in depressed patients with and without a history of suicidal behavior.

Method

Functional magnetic resonance imaging was used to measure brain activation during the Go/No-Go response inhibition task in 25 unmedicated and depressed middle-aged suicide attempters, 22 unmedicated depressed patient controls with no personal or family history of suicidal behavior, and 27 healthy controls. Whole-brain analyses were conducted with SPM12.

Results

Suicide attempters exhibited an elevated number of commission errors relative to both control groups. However, suicide attempters did not differ from patient controls in terms of brain activation for any contrast. Analyses showed a significant association between depression and brain activation in the left inferior frontal gyrus and medial thalamus during Go v. No-Go, and in the bilateral parietal cortex and left orbitofrontal cortex during No-Go v. baseline. These regions were correlated with psychological pain, suicidal ideation and global functioning. There was no association between brain activation and personal histories of suicidal act.

Conclusions

Our study suggests that deficits in cognitive inhibition, in relation to the inferior frontal gyrus, thalamus, orbitofrontal cortex and parietal cortex, are related to the depressive state and not specifically to suicide vulnerability. We hypothesize that state-related deficits may add to trait-like cognitive impairments to facilitate suicidal acts. These different types of cognitive impairments may necessitate different therapeutic strategies for the prevention of suicide.

Keywords

Cognitive inhibitiondepressionfunctional magnetic resonance imagingGo/No-Go testsuicide
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 5 , April 2016 , pp. 933 - 944
Copyright
Copyright © Cambridge University Press 2015 

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

Barch, DM, Braver, TS, Carter, CS, Poldrack, RA, Robbins, TW (2009). CNTRICS final task selection: executive control. Schizophrenia Bulletin 35, 115–135.CrossRefGoogle ScholarPubMed
Barratt, ES (1965). Factor analysis of some psychometric measures of impulsiveness and anxiety. Psychological Reports 16, 547–554.CrossRefGoogle ScholarPubMed
Beardsall, L, Brayne, C (1990). Estimation of verbal intelligence in an elderly community: a prediction analysis using a shortened NART. British Journal of Clinical Psychology 29, 83–90.CrossRefGoogle Scholar
Bechara, A, Damasio, H, Damasio, AR, Lee, GP (1999). Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. Journal of Neuroscience 19, 5473–5481.CrossRefGoogle ScholarPubMed
Beck, AT, Kovacs, M, Weissman, A (1979). Assessment of suicidal intention: the Scale for Suicide Ideation. Journal of Consulting and Clinical Psychology 47, 343–352.CrossRefGoogle ScholarPubMed
Beck, AT, Schuyler, D, Herman, I (1974). Development of suicidal intent scales. In The Prediction of Suicide (ed. Beck, HLP Resnik, AT and Lettieri, DJ), pp. 45–56. Charles Press: Bowie, MD.Google Scholar
Botvinick, MM, Braver, TS, Barch, DM, Carter, CS, Cohen, JD (2001). Conflict monitoring and cognitive control. Psychological Review 108, 624–652.CrossRefGoogle ScholarPubMed
Brown, GL, Goodwin, FK (1986). Human aggression and suicide. Suicide and Life Threatening Behavior 16, 223–243.CrossRefGoogle ScholarPubMed
Burgess, PW, Shallice, T (1996). Response suppression, initiation and strategy use following frontal lobe lesions. Neuropsychologia 34, 263–272.CrossRefGoogle ScholarPubMed
Buss, AH, Durkee, A (1957). An inventory for assessing different kinds of hostility. Journal of Consulting Psychology 21, 343–349.CrossRefGoogle ScholarPubMed
Chikazoe, J (2010). Localizing performance of go/no-go tasks to prefrontal cortical subregions. Current Opinion in Psychiatry 23, 267–272.CrossRefGoogle ScholarPubMed
Criaud, M, Boulinguez, P (2013). Have we been asking the right questions when assessing response inhibition in go/no-go tasks with fMRI? A meta-analysis and critical review. Neuroscience and Biobehavioral Reviews 37, 11–23.CrossRefGoogle ScholarPubMed
Dodds, CM, Morein-Zamir, S, Robbins, TW (2011). Dissociating inhibition, attention, and response control in the frontoparietal network using functional magnetic resonance imaging. Cerebral Cortex 21, 1155–1165.CrossRefGoogle ScholarPubMed
Duann, JR, Ide, JS, Luo, X, Li, CS (2009). Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. Journal of Neuroscience 29, 10171–10179.CrossRefGoogle ScholarPubMed
First, MB, Gibbon, M, Spitzer, RL, Williams, JBW, Benjamin, LS (1997). Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II). American Psychiatric Press Inc.: Washington, DC.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition with Psychotic Screen. Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Friston, KJ, Frith, CD, Frackowiak, RS, Turner, R (1995). Characterizing dynamic brain responses with fMRI: a multivariate approach. NeuroImage 2, 166–172.CrossRefGoogle ScholarPubMed
Garavan, H, Ross, TJ, Murphy, K, Roche, RA, Stein, EA (2002). Dissociable executive functions in the dynamic control of behavior: inhibition, error detection, and correction. NeuroImage 17, 1820–1829.CrossRefGoogle ScholarPubMed
Godefroy, O, La GREFEX (Groupe de Réflexion pour l'Evaluation des Fonctions Exécutives) (2008). Fonctions exécutives et pathologies neurologiques et psychiatriques: evaluation en pratique clinique (Executive Functions and Neurological and Psychiatric Pathologies: Evaluation in Clinical Practice). Solal Editions: Marseille.Google Scholar
Gorlyn, M, Keilp, JG, Oquendo, MA, Burke, AK, Mann, JJ (2013). Iowa Gambling Task performance in currently depressed suicide attempters. Psychiatry Research 207, 150–157.CrossRefGoogle ScholarPubMed
Graf, H, Abler, B, Freudenmann, R, Beschoner, P, Schaeffeler, E, Spitzer, M, Schwab, M, Gron, G (2011). Neural correlates of error monitoring modulated by atomoxetine in healthy volunteers. Biological Psychiatry 69, 890–897.CrossRefGoogle ScholarPubMed
Graham, J, Salimi-Khorshidi, G, Hagan, C, Walsh, N, Goodyer, I, Lennox, B, Suckling, J (2013). Meta-analytic evidence for neuroimaging models of depression: state or trait? Journal of Affective Disorders 151, 423–431.CrossRefGoogle ScholarPubMed
Guy, W (2000). Clinical Global Impressions (CGI) Scale. Modified From: Rush J, et al.: Psychiatric Measures. APA: Washington, DC.Google Scholar
Hamilton, M (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology 32, 50–55.CrossRefGoogle ScholarPubMed
Hamilton, MA (1960). Rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Hampshire, A, Chamberlain, SR, Monti, MM, Duncan, J, Owen, AM (2010). The role of the right inferior frontal gyrus: inhibition and attentional control. NeuroImage 50, 1313–1319.CrossRefGoogle ScholarPubMed
Hoehne, A, Richard-Devantoy, S, Ding, Y, Turecki, G, Jollant, F (2015). First-degree relatives of suicide completers may have impaired decision-making but functional cognitive control. Journal of Psychiatric Research 68, 192–197.CrossRefGoogle ScholarPubMed
Jollant, F, Bellivier, F, Leboyer, M, Astruc, B, Torres, S, Verdier, R, Castelnau, D, Malafosse, A, Courtet, P (2005). Impaired decision making in suicide attempters. American Journal of Psychiatry 162, 304–310.CrossRefGoogle ScholarPubMed
Jollant, F, Lawrence, NL, Olie, E, Guillaume, S, Courtet, P (2011). The suicidal mind and brain: a review of neuropsychological and neuroimaging studies. World Journal of Biological Psychiatry 12, 319–339.CrossRefGoogle ScholarPubMed
Keilp, JG, Gorlyn, M, Oquendo, MA, Burke, AK, Mann, JJ (2008). Attention deficit in depressed suicide attempters. Psychiatry Research 159, 7–17.CrossRefGoogle ScholarPubMed
Keilp, JG, Gorlyn, M, Russell, M, Oquendo, MA, Burke, AK, Harkavy-Friedman, J, Mann, JJ (2013). Neuropsychological function and suicidal behavior: attention control, memory and executive dysfunction in suicide attempt. Psychological Medicine 43, 539–551.CrossRefGoogle ScholarPubMed
Keilp, JG, Sackeim, HA, Brodsky, BS, Oquendo, MA, Malone, KM, Mann, JJ (2001). Neuropsychological dysfunction in depressed suicide attempters. American Journal of Psychiatry 158, 735–741.CrossRefGoogle ScholarPubMed
Mackinnon, A, Mulligan, R (2005). The estimation of premorbid intelligence levels in French speakers [article in French]. Encephale 31, 31–43.CrossRefGoogle ScholarPubMed
Mann, JJ (2003). Neurobiology of suicidal behaviour. Nature Reviews Neuroscience 4, 819–828.CrossRefGoogle ScholarPubMed
Miller, EK, Cohen, JD (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 24, 167–202.CrossRefGoogle ScholarPubMed
Mostofsky, SH, Simmonds, DJ (2008). Response inhibition and response selection: two sides of the same coin. Journal of Cognitive Neuroscience 20, 751–761.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Olie, E, Guillaume, S, Jaussent, I, Courtet, P, Jollant, F (2010). Higher psychological pain during a major depressive episode may be a factor of vulnerability to suicidal ideation and act. Journal of Affective Disorders 120, 226–230.CrossRefGoogle Scholar
Pan, LA, Batezati-Alves, SC, Almeida, JR, Segreti, A, Akkal, D, Hassel, S, Lakdawala, S, Brent, DA, Phillips, ML (2011). Dissociable patterns of neural activity during response inhibition in depressed adolescents with and without suicidal behavior. Journal of the American Academy of Child and Adolescent Psychiatry 50, 602–611.e603.CrossRefGoogle ScholarPubMed
Posner, K, Oquendo, MA, Gould, M, Stanley, B, Davies, M (2007). Columbia Classification Algorithm of Suicide Assessment (C-CASA): classification of suicidal events in the FDA's pediatric suicidal risk analysis of antidepressants. American Journal of Psychiatry 164, 1035–1043.CrossRefGoogle ScholarPubMed
Raust, A, Slama, F, Mathieu, F, Roy, I, Chenu, A, Koncke, D, Fouques, D, Jollant, F, Jouvent, E, Courtet, P, Leboyer, M, Bellivier, F (2007). Prefrontal cortex dysfunction in patients with suicidal behavior. Psychological Medicine 37, 411–419.CrossRefGoogle ScholarPubMed
Richard-Devantoy, S, Berlim, MT, Jollant, F (2014 a). A meta-analysis of neuropsychological markers of vulnerability to suicidal behavior in mood disorders. Psychological Medicine 44, 1663–1673.CrossRefGoogle ScholarPubMed
Richard-Devantoy, S, Berlim, MT, Jollant, F (2014 b). Suicidal behaviour and memory: a systematic review and meta-analysis. World Journal of Biological Psychiatry. Published online 12 August 2014. doi:10.3109/15622975.2014.925584.Google ScholarPubMed
Richard-Devantoy, S, Gorwood, P, Annweiler, C, Olie, JP, Le Gall, D, Beauchet, O (2012 a). Suicidal behaviours in affective disorders: a deficit of cognitive inhibition? Canadian Journal of Psychiatry 57, 254–262.CrossRefGoogle ScholarPubMed
Richard-Devantoy, S, Jollant, F, Kefi, Z, Turecki, G, Olie, JP, Annweiler, C, Beauchet, O, Le Gall, D (2012 b). Deficit of cognitive inhibition in depressed elderly: a neurocognitive marker of suicidal risk. Journal of Affective Disorders 140, 193–199.CrossRefGoogle ScholarPubMed
Richard-Devantoy, S, Szanto, K, Butters, MA, Kalkus, J, Dombrovski, AY (2015). Cognitive inhibition in older high-lethality suicide attempters. International Journal of Geriatric Psychiatry 30, 274–283.CrossRefGoogle ScholarPubMed
Shallice, T, Burgess, PW (1991). Deficits in strategy application following frontal lobe damage in man. Brain 114, 727–741.CrossRefGoogle ScholarPubMed
Simmonds, DJ, Pekar, JJ, Mostofsky, SH (2008). Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 46, 224–232.CrossRefGoogle ScholarPubMed
Simoes-Franklin, C, Hester, R, Shpaner, M, Foxe, JJ, Garavan, H (2010). Executive function and error detection: the effect of motivation on cingulate and ventral striatum activity. Human Brain Mapping 31, 458–469.CrossRefGoogle ScholarPubMed
Spielberger (1983). Manual for the State-Trait Anxiety Inventory (Form Y). Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Stroop, JR (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology 6, 643–661.CrossRefGoogle Scholar
Swick, D, Ashley, V, Turken, U (2011). Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. NeuroImage 56, 1655–1665.CrossRefGoogle Scholar
Turecki, G, Ernst, C, Jollant, F, Labonte, B, Mechawar, N (2012). The neurodevelopmental origins of suicidal behavior. Trends in Neurosciences 35, 14–23.CrossRefGoogle ScholarPubMed
Vallesi, A, McIntosh, AR, Alexander, MP, Stuss, DT (2009). fMRI evidence of a functional network setting the criteria for withholding a response. NeuroImage 45, 537–548.CrossRefGoogle ScholarPubMed
Wechsler, D (2008). Wechsler Adult Intelligence Scale: Technical and Interpretive Manual. The Psychological Corporation: San Antonio, TX.Google Scholar
Supplementary material: File

Richard-Devantoy supplementary material

Richard-Devantoy supplementary material 1

Download Richard-Devantoy supplementary material(File)
File 7.7 MB