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A meta-analysis of neuropsychological markers of vulnerability to suicidal

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Psychological Medicine, Page 1 of 11. © Cambridge University Press 2013 OR I G I N A L A R T I C L E
doi:10.1017/S0033291713002304

A meta-analysis of neuropsychological markers of

vulnerability to suicidal behavior in mood disorders

S. Richard-Devantoy1,2, M. T. Berlim1 and F. Jollant1*

1
McGill University, Department of Psychiatry and Douglas Mental Health University Institute, McGill Group for Suicide Studies, Montréal
(Québec), Canada
2
Laboratoire de Psychologie des Pays de la Loire EA 4638, Université de Nantes et Angers, France

Background. Suicidal behavior results from a complex interplay between stressful events and vulnerability factors,
including cognitive deficits. However, it is not clear which cognitive tests may best reveal this vulnerability. The objective
was to identify neuropsychological tests of vulnerability to suicidal acts in patients with mood disorders.

Method. A search was made of Medline, EMBASE and PsycINFO databases, and article references. A total of 25 studies
(2323 participants) met the selection criteria. A total of seven neuropsychological tests [Iowa gambling task (IGT),
Stroop test, trail making test part B, Wisconsin card sorting test, category and semantic verbal fluencies, and continuous
performance test] were used in at least three studies to be analysed.

Results. IGT and category verbal fluency performances were lower in suicide attempters than in patient controls
[respectively, g = –0.47, 95% confidence interval (CI) –0.65 to –0.29 and g = –0.32, 95% CI –0.60 to –0.04] and healthy con-
trols, with no difference between the last two groups. Stroop performance was lower in suicide attempters than in patient
controls (g = 0.37, 95% CI 0.10–0.63) and healthy controls, with patient controls scoring lower than healthy controls.
The four other tests were altered in both patient groups versus healthy controls but did not differ between patient groups.

Conclusions. Deficits in decision-making, category verbal fluency and the Stroop interference test were associated with
histories of suicidal behavior in patients with mood disorders. Altered value-based and cognitive control processes may
be important factors of suicidal vulnerability. These tests may also have the potential of guiding therapeutic interventions
and becoming part of future systematic assessment of suicide risk.

Received 26 April 2013; Revised 7 August 2013; Accepted 10 August 2013

Key words: Cognitive control, decision making, mood disorders, neuropsychology, suicidal behaviour, vulnerability.

Introduction It is generally agreed that suicidal behaviors may

be best modeled as the interplay between vulnerability
According to the World Health Organization, suicide
and contextual factors, including proximal stressful
accounts for more than 1 million yearly deaths world-
events, acute mental disorder like major depression,
wide (http://www.who.int/topics/suicide/en/) and is
alcohol intake or physical pain (Mann, 2003). This
one of the leading causes of preventable premature
model has been strongly supported by clinical, cellular,
deaths. In addition, 10 to 20 times more individuals
molecular and genetic studies (Mann, 2003) and, more
engage in non-fatal suicidal acts, currently the most
recently, by neuropsychological and neuroimaging
predictive risk factor for future suicide (Oquendo
studies (Jollant et al. 2011).
et al. 2004). To date, the prevention of suicidal be-
Neurocognitive alterations represent relevant vul-
haviors remains difficult partly due to the fact that
nerability factors and potential endophenotypes of
the complex processes underlying the triggering and
suicidal behavior. Indeed, several recent publications
development of a suicidal crisis in a given individual
have reported cognitive deficits in patients with a
are not fully understood. As a consequence, tools to
history of suicidal acts compared with non-suicidal
detect high-risk subjects are insufficient and interven-
patients and healthy controls (Jollant et al. 2011).
tions specifically targeting suicidal risk are lacking.
Moreover, some deficits, like disadvantageous decision-
making, have been found in remitted patients (Jollant
et al. 2005) and to be influenced by an interaction
between early adverse events and genetic variants
* Address for correspondence: Dr F. Jollant, Douglas Mental Health
University Institute, Frank B. Common Building, 6875 LaSalle
(Guillaume et al. 2012) while others [as measured
Boulevard, Montréal (Québec), H4H 1R3, Canada. by the Wisconsin card sorting test (WCST)] have
(Email: fabrice.jollant@mcgill.ca) been shown in relatives of suicide completers
2 S. Richard-Devantoy et al.
(McGirr et al. 2013). Apart from improving our under-
standing of the suicidal vulnerability, these cognitive
deficits could be both measurable markers of vulner-
ability and the target of future therapeutic interventions
aimed at reducing the long-term risk of suicidal acts.
There is a need to synthesize evidence from cumu-
lating literature on cognitive deficits in suicide attemp-
ters in order to determine which neuropsychological
tests reveal impairments more strongly associated with
a history of suicidal act, i.e. a higher risk of recurrence
of suicidal acts and completed suicide. It is notably
important to disentangle the cognitive deficits associ-
ated with suicidal behavior from those more closely
related to co-morbid disorders such as major de-
pression. In the current paper, we systematically re-
viewed the literature on the neuropsychology of
suicidal behavior, and conducted a meta-analysis
to explore putative cognitive markers of suicidal
vulnerability.
Method
Data sources
An English and French systematic literature search of
Medline, EMBASE and PsycINFO databases was per-
formed for human studies published from 1 January
1960 to 31 March 2013. The medical subject heading
(MeSH) term ‘suicide’ was combined with the MeSH
terms ‘cognition’, ‘neuropsychology’, ‘neuropsycho-
logical tests’, ‘executive function’, ‘decision making’,
‘problem solving’, ‘prefrontal cortex’, and with the
title/abstract (TIAB) terms ‘neuropsychological func-
tions’, ‘executive functioning’ and ‘executive perform-
ance’. An iterative process was used to ensure that all
relevant articles were obtained. A further hand search
of the bibliographical references of the selected papers
and existing reviews was conducted to identify
additional potential studies. References were also
selected from our research group’s online database
(www.bdsuicide.disten.com).
Study selection
Abstract selection was based on the STrengthening the
Reporting of OBservational studies in Epidemiology
(STROBE) checklist (Von Elm et al. 2008) which de-
scribes items that should be included in reports of
cohort studies. Abstracts identified through the litera-
ture search were independently evaluated by two
reviewers (S.R.-D. and F.J.) and selected by a consensus
from all authors.
Studies that met the following inclusion criteria were
included in this meta-analysis: (1) published in an
English or French language peer-reviewed journal;
(2) included at least one neuropsychological task;
(3) compared at least two groups of which one com-
prised patients with a history of suicide attempt
(defined as any act carried out with a certain intent
to die and different from non-suicidal self-injury;
Mann, 2003); and (4) included patients who suffered
from mood disorders (both unipolar or bipolar) but
not schizophrenia or other major psychiatric disorder
diagnosed according to the Diagnostic and Statistical
Manual of Mental Disorders, fourth edition, text revi-
sion (DSM-IV-TR) criteria. We focused on mood dis-
orders as more studies have been published in this
domain and to limit heterogeneity in studied popu-
lations. Full articles were then obtained for final
analyses.
Of the 1830 originally identified abstracts, 25 studies
met the inclusion criteria (Bartfai et al. 1990; Ellis et al.
1992; Becker et al. 1999; King et al. 2000; Keilp et al.
2001, 2013; Audenaert et al. 2002; Jollant et al. 2005,
2010; LeGris et al., 2012; Raust et al. 2007; Westheide
et al. 2008; Yen et al. 2008; Malloy-Diniz et al. 2009;
Oldershaw et al. 2009; Cha et al. 2010; Martino et al.
2010; Gilbert et al. 2011; Richard-Devantoy et al. 2011,
2012, 2013a; Bridge et al. 2012; McGirr et al. 2012;
Miranda et al. 2012; Gorlyn et al. 2013). Although
eligible, three studies were not included, or only
partially (for instance, some tests but not others),
because precise means and standard deviations were
not available in papers and could not be obtained
after contacting the authors (Williams & Broadbent,
1986; Dombrovski et al. 2008; Gilbert et al. 2011).
Finally, one study which assessed patients with border-
line personality disorder was also included as levels of
depression and rates of co-morbid mood disorders
were high (LeGris et al. 2012).
The quality of each study was assessed indepen-
dently by two reviewers (S.R.-D. and F.J.) using the
Crombie criteria adapted by Petticrew & Roberts
(2006).
Data extraction and analyses
A standardized form was used to extract data, which
included authors, date of publication, study design,
settings, study population, cognitive tests used, defi-
nition of suicidal behavior, and neuropsychological
scores (means and standard deviations).
Only tasks that were used in at least three separate
studies were included in the analyses. Overall, seven
neuropsychological tests were analysed as they met
this criterion: (1) Iowa gambling task (IGT; net score
= number of advantageous minus disadvantageous
choices); (2) Stroop test (Stroop; interference score,
i.e. time to read the color–word interference sheet
minus time to name the color of each block sheet);
(3) trail-making test part B (TMTB; time completion);
 Neuropsychological markers of vulnerability to suicidal behavior 3
(4) WCST (perseverative errors); (5) FAS semantic
verbal fluency test (number of words); (6) categorical
verbal fluency test (Animals; number of words); and
(7) continuous performance test (CPT; commission
errors).
Analyses were performed using Comprehensive
Meta-Analyses version 2.0 (Biostat, USA), and IBM
SPSS version 20 (IBM Corporation, USA) software.
Three groups were compared: suicide attempters
(patients with a history of suicide attempt), patient
controls (i.e. patients with no personal history of
suicidal act) and healthy controls. When two groups
of suicide attempters were reported in one study
[e.g. low versus high lethality (McGirr et al. 2012,
Keilp et al. 2013) or violent versus non-violent (Jollant
et al. 2005)], the combined means and standard devi-
ations were calculated to obtain a global group, using
the following formula:
NX μX + NY μY
μX<Y = , moderate effect sizes. The fail-safe N, i.e. the number
NX + NY

















































NX σ 2X + NY σ 2Y NX NY
σ X<Y = + + (μX − μY )2 .
NX + NY (NX + NY )2
We performed a meta-analysis of aggregate data
and used a random-effects model as we assumed
that the true effect sizes had probably varied between
the included studies (Riley et al. 2011). Pooled Hedges’
g effect sizes for subjects’ neuropsychological scores
and depression ratings were computed (Hedges &
Olkin, 1985). Qualitative descriptors of the obtained
effect sizes are usually considered small if <0.3, moder-
ate if between 0.4–0.8, and large if >0.8 (Egger et al.
2001).
Heterogeneity was assessed using the Q statistics
and the I2 index (Cooper et al. 2009). Values of p < 0.10
for the former and >35% for the latter were deemed
as indicative of study heterogeneity. Finally, we used
funnel plots, Rosenthal’s fail-safe N (Rosenthal, 1979)
and Egger’s regression intercept (Egger et al. 1997) to
test for the presence of publication bias (Cooper et al.
2009).
Results
A total of 25 studies were included (Table 1) comprising
2323 participants, of whom 831 were suicide attempters
[mean age = 40.5 years, S.D. = 9.4 years; 43.6% males;
75.4%, 95% confidence interval (CI) 15–100% unipolar
disorder; 52.4%, 95% CI 15–100% bipolar disorder],
824 patient controls (mean age = 41.6 years, S.D. = 9.4
years; 41.0% males; 77.2%, 95% CI 3–100% unipolar dis-
order; 54.9%, 95% CI 17–100% bipolar disorder], and
668 healthy controls (mean age 39.2 years, S.D. = 9.5
years; 50.8% males). In 18 studies, patients were
under a psychotropic medication; in four studies,
patients did not have any medication (Keilp et al.
2001, 2013; Jollant et al. 2005; Gorlyn et al. 2013), and
data were not available for three studies even after con-
tacting the authors (Bartfai et al. 1990; Ellis et al. 1992;
Becker et al. 1999).
Table 2 presents the results of the contrasts between
the three groups for the seven neuropsychological
tests, and Table 3 provides a summary of the main
findings. Detailed information on heterogeneity and
publication bias can be found in the online Sup-
plementary material.
Suicide attempters versus patient controls
Suicide attempters had significantly lower IGT net
scores and Animals scores, and lower Stroop perform-
ance than patient controls (Fig. 1), all representing
of unpublished or missing null findings that would
be needed to render the results non-significant, was
60 for the IGT, five for the Animals and 29 for the
Stroop. Mean age, gender, depression level, and the
proportion of unipolar/bipolar disorders did not differ
between the two groups for any test, thus ruling out
these variables as confounding factors. Regarding
Stroop, results were significant whether assessing the
traditional version only or including the emotional
version.
Heterogeneity exceeded that expected by chance at
p < 0.05 only for the Stroop and TMTB, implying that
the variance among the effect sizes was greater than
expected by sampling error (online Supplementary
Table S1). The study by Richard-Devantoy et al.
(2011) was probably responsible for the heterogeneity
related to the Stroop, and the studies by Ellis et al.
(1992) and Yen et al. (2008) for the TMTB. After exclud-
ing these studies, the heterogeneity disappeared and
the main results remained significant.
The funnel plots were reasonably symmetrical for
all neuropsychological tests except for the CPT, sug-
gesting a low risk of publication bias. Nevertheless,
the more conservative Egger’s regression intercept
suggested no publication bias.
Suicide attempters versus healthy controls
Suicide attempters had significantly lower perform-
ance than healthy controls on all seven neuropsycho-
logical tasks, all with moderate to high effect sizes.
The fail-safe N was 100 for the IGT, 96 for the
Stroop, 26 for the TMTB, 27 for the WCST, 44 for the
FAS, 36 for Animals, and seven for the CPT. Mean
age and gender did not differ between the two groups,
 4 S. Richard-Devantoy et al.
Table 1. Studies included in the meta-analysis

Suicide attempters Patient controls Healthy controls

Mean Mean
Age, years Males, depression UP, BP, Age, years Males, depression UP, BP, Mean age, Males, Neuropsychological
Study n (S.D.) % score (S.D.)a M % % n (S.D.) % score (S.D.)a M % % n years (S.D.) % tests

Audenaert et al. (2002) 10 31.9 (10.9) 50 27.8 (3.0)b Y 100 0 10 21.8 (2.0) 40 FAS, Animals
Bartfai et al. (1990) 9 33.0 100 N.A. N.A. 22.2 22.2 7 30.0 100 N.A. N .A . N .A . N.A. 8 28.0 100 WCST
Becker et al. (1999) 31 38.4 (16.2) 35.4 20.8 (11.9)c N.A. N.A. N.A. 31 38.2 (14.6) 35.4 10.6 (8.6)c N .A . N .A . N.A. Stroop
Bridge et al. (2012) 40 15.5 (1.4) 25 12.8 (8.3)d Y 75 40 15.6 (1.4) 25 13.5 (13.3)d 40 IGT
Cha et al. (2010) 68 34.1 (10.5) 57.4 N.A. Y 85.3 56 35.2 (13.2) 64.8 N.A. Y 62.5 Stroop
Ellis et al. (1992) 20 30.4 30 17.3 (13.3)c N.A. 55 N.A. 27 40.0 26 17.4 (13.0)c N .A . 85 33 TMT, WCST
Gilbert et al. (2011) 28 43.7 (10.7) 50 8.6 (7.5)b Y 0 100 39 41.1 (12) 59 10.7 (6.9)b Y 0 100 IGT, Stroop (N/A),
TMTB (N/A),
WCST (N/A), FAS
(N/A), Animals (N/A)
Gorlyn et al. (2013) 26 35.0 (11.9) 65 25.8 (6.84)b N 69.4 30.6 46 37.7 (10.7) 32.6 25.6 (7.2)b N 78.8 21.3 42 32.3 (10.6) 61.9 IGT
Jollant et al. (2005) 69 43.0 (11.8) 49 N.A. Y 70.5 26.1 25 40.4 (12.2) 35 N.A. Y 72 28 82 38.8 (9.1) 73.2 IGT
Jollant et al. (2010) 13 40.3 (11.3) 100 2.4 (2.3)b N 100 0 12 43.6 (10.7) 100 2.8 (2.3)b N 100 0 15 32.6 (10.1) 100 IGT
Keilp et al. (2001) 29 38.5 (10.6) 37.8 29.3 (5.2)b N 73.3 0 21 41 (10.9) 57.1 27.5 (6.4)b N 81 0 22 41.2 (16.8) 63.6 Stroop, TMTB, WCST,
FAS, Animals, CPT
Keilp et al. (2013) 72 35.7 (11.6) 36 25.7 (7.3)b N 50 22 80 40.1 (11.9) 47.5 25.6 (7.4)b N 63 17 56 31.5 (11.1) 50 Stroop, TMTB, WCST,
FAS, Animals, CPT
King et al. (2000) 18 66.7 (10.1) 44 28.1 (8.36)b Y 100 0 29 64.2 (10.9) 31 29.5 (8.6)b Y 100 0 30 N.A. N.A. TMT, WCST, FAS
LeGris et al. (2012) 13 32.2 (10.5) 0 N.A. Y – – 13 32.2 (10.5) 0 N/A Y – – 41 31.2 (9.0) 0 IGT, Stroop
Malloy-Diniz et al. 18 41 (13.8) 33.3 9.6 (5.1)c Y 0 100 21 40.8 (12.6) 47.6 8.0 (4.3)c Y 0 100 50 36.9 (9.8) 33.3 IGT, Stroop, WCST, CPT
(2009)
Martino et al. (2010) 22 42.1 (10.6) 21.5 2.4 (1.9)b Y 0 100 63 39.2 (10.8) 39.4 2.0 (2.0)b Y 0 100 34 40 (12.9) 35.3 IGT (N/A), TMTB,
WCST, FAS
McGirr et al. (2012) 34 67.8 (7.84) 50 22.3 (5.2)b Y 100 0 29 70.3 (9.0) 34.4 19.85 (3.6)b Y 100 0 30 69.7 (6.8) 53.3 WCST
Miranda et al. (2012) 13 18.3 (0.6) 8 14.3 (9.1)c Y 15 15 32 18.31 (0.8) 28 14.12 (9.0)c Y 3 0 WCST
Oldershaw et al. (2009) 54 15.8 (1.5) 9.3 N.A. Y 100 0 22 15.7 (1.3) 9.1 N.A. Y 100 0 57 15.8 (1.5) 19.3 IGT
Raust et al. (2007) 30 39.8 (13.6) 40 3.6 (2.8)e Y 50 27 39 44.6 (12.4) 54 Stroop
Richard-Devantoy et al. 10 75.3 (2.3) 30 28.1 (0.6)b Y 100 0 10 72.9 (1.3) 30 27.7 (2)b Y 100 0 Stroop
(2011)
 Neuropsychological markers of vulnerability to suicidal behavior 5

except for the TMTB with more men among the healthy
controls compared with the suicide attempters.
Heterogeneity exceeded that expected by chance for

TMT, WCST, CPT

S.D., Standard deviation; M, medication; UP, unipolar disorder; BP, bipolar disorder; Y, yes; FAS, FAS verbal fluency test; Animals, animal verbal fluency test; N.A., data not
all tests except for the FAS and Animals. No specific
FAS, Animals
Stroop, TMTB,

FAS, Animals

IGT, CPT study or set of studies was identified as being probably

responsible for the heterogeneity associated with data
on the IGT. The studies by Richard-Devantoy et al.

available; WCST, Wisconsin card sorting test; IGT, Iowa gambling task; TMT, trail-making test; TMTB, trail-making test part B; CPT, continuous performance test.
(2012) and Malloy-Diniz et al. (2009) were probably
responsible for the heterogeneity related to the
35.1

N.A.
40

Stroop, the studies by Richard-Devantoy et al. (2012)

and Martino et al. (2010) for the TMTB, the study by
42.7 (11.3)
75.2 (3.4)

39 (10.9)

Malloy-Diniz et al. (2009) for the WCST, and the

study by Keilp et al. (2001) for the CPT (2013). After
excluding those studies, the heterogeneity of each
20

37

29

neuropsychological test disappeared but the main

23.3

100

results remained significant.

0

The associated funnel plots were reasonably sym-

73.3
100

metrical for all neuropsychological tests. Egger’s re-

0

gression intercept test suggested no publication bias.

Y

Y
2.97 (2.58)b
28.3 (2.4)b

Patient controls versus healthy controls

N/A

Depression scores come from different scales and, therefore, cannot be directly compared across studies:

Patient controls had significantly lower performance

on the Stroop, TMTB and FAS than healthy controls,
50.6
40

29

all with moderate effect sizes. Fail-safe N’s were 40,

40 and 33, respectively. Mean age and gender did
40.9 (11.0)

41.4 (12.9)
75.9 (6.7)

not differ between the two groups except for the

Stroop. Compared with healthy controls, patient con-
trols were older. In addition, the heterogeneity
20

33.3 31

87

exceeded that expected by chance for this task. The

100

study by Keilp et al. (2013) was probably responsible

0

for the heterogeneity related to the Stroop task. After

66.7
100

100

excluding this study, the heterogeneity disappeared

0

and the difference in age and gender was not signifi-

Y

Y
Y

cant anymore.
Heterogeneity exceeded that expected by chance for
27.7 (3.5)b

4.6 (2.6)b

MADRS: Montgomery–Asberg Depression Rating Scale.

the IGT, Stroop, TMTB, WCST and CPT. The studies by

15 (1)b
N/A

Martino et al. (2010) and Oldershaw et al. (2009) were

probably responsible for the heterogeneity related to
the IGT, whereas the studies by Richard-Devantoy
37.1

66.7
N.A.
45

et al. (2012) and Keilp et al. (2013), and the studies by

Keilp et al. (2013) and Malloy-Diniz et al. (2009), were
43.3 (10.6)
77.1 (7.2)

34.8 (8.3)

probably responsible for the heterogeneity related to

37.3 (11)

the TMTB and the Stroop, respectively. After excluding

those studies, the heterogeneity disappeared but the
Hamilton Depression Scale.

Beck Depression Inventory.

Beck Depression Inventory.
9
20

35

29

main results remained significant. The studies by

King et al. (2000) and Malloy-Diniz et al. (2009) were
probably responsible for the heterogeneity related to
Richard-Devantoy et al.

Richard-Devantoy et al.

Westheide et al. (2008)

the WCST, and the study by Keilp et al. (2001, 2013)

for the heterogeneity related to the CPT. After their
Yen et al. (2008)

exclusion, the heterogeneity disappeared and the con-

trasts became significant.
(2013a)
(2012)

The associated funnel plots were reasonably sym-

d
b
a

e
c

metrical for all variables, although Egger’s regression

 6 S. Richard-Devantoy et al.

intercept test suggested a possible publication bias for

1.7 (*)
1.9 (*)
−5.0***
2.1**
2.8**

CI, Confidence interval; IGT, Iowa gambling task; Animals, animal verbal fluency test; TMTB, trail-making test part B; FAS, FAS verbal fluency test; WCST, Wisconsin card sorting
−1.6
−1.8
the TMTB.

Za
Discussion

−0.49 (−0.67 to −0.29)

−0.24 (−0.53 to 0.05)
−0.30 (−0.63 to 0.04)

0.30 (−0.05 to 0.66)

To our knowledge, this is the first meta-analysis

0.4 (−0.01 to 0.82)

Pooled Hedges’ g

0.73 (0.22 to 1.23)

Patients controls v. healthy controls

0.8 (0.05 to 1.50)

on neuropsychological tests associated with vulner-
ability to suicidal behavior. We report here that per-
(95% CI)

formance on the IGT, Animals and Stroop was

significantly altered in patients with a history of suicide
attempts relative to those without such history. Hedges’
g effect sizes were moderate (0.47, 0.37 and 0.32, respect-
ively), which is particularly relevant considering the
fact that we are comparing two patient groups. IGT
321 v. 218
152 v. 135
155 v. 189
213 v. 162
244 v. 199
250 v. 230
122 v. 128
and Animals scores were found to be significantly
different between suicide attempters and both control
n

groups, but not between patient controls and healthy

Table 2. Effect sizes for the contrasts between suicide attempters, patient controls and healthy controls for the seven neuropsychological tests

controls, suggesting that the measured deficits are

−3.6***
3.8***
3.6***

associated with the vulnerability to suicidal behavior

−3.3**

2.2**

2.9**
2.3*
Za

but not with co-morbid mood disorders. In the case of

* p < 0.05, ** p < 0.01, *** p < 0.001, (*) contrast became significant after excluding studies responsible for heterogeneity.

the Stroop, however, a reduced performance was also

found in patient controls versus healthy controls,
−0.65 (−1.03 to −0.27)
−0.67 (−1.02 to −0.33)

−0.53 (−0.82 to −0.24)

Suicide attempters v. healthy controls

suggesting a shared vulnerability to suicidal behavior

Pooled Hedges’ g

0.91 (0.41 to 1.42)

0.63 (0.07 to 1.19)

0.44 (0.15 to 0.74)

and mood disorders, with greater alterations observed

0.7 (0.09 to 1.30)

in suicide attempters. Finally, other tests including the

TMTB, WCST, FAS and CPT seemed to be more closely
(95% CI)

associated with mood disorders than suicidal behavior.

It is important to point out that these latter alterations
were also found in suicide attempters versus healthy
controls. Therefore, although they did not seem to be
250 v. 350
166 v. 145
198 v. 228
161 v. 162
206 v. 209
202 v. 230
119 v. 128

specifically related to suicidal behavior, they should

be considered as part of the general set of cognitive
deficits experienced by these patients.
n

Findings from this meta-analysis have three main

implications. First, they indicate directions for the
−5.1***

understanding of suicidal behaviors. Although no neu-

2.7**
−2.2*

−0.8
−1.0
0.1
1.7
Za

ropsychological test is specific to a cognitive function or

brain region, our results suggest that suicide attempters
display alterations affecting their ability to make
−0.47 (−0.65 to −0.29)
−0.32 (−0.60 to −0.04)

decisions in conditions of uncertainty (Bechara et al.

Suicide attempters v. patient controls

−0.13 (−0.46 to 0.18)

0.02 (−0.21 to 0.24)

0.14 (−0.09 to 0.37)
−0.1 (−0.29 to 0.08)
Pooled Hedges’ g

0.37 (0.10 to 0.63)

1999), to generate words restricted to a given category

(Harrison et al. 2000) and to override automatic
Test for the significance of the effect size.

responses (MacLeod, 1991). It cannot be completely

(95% CI)

test; CPT, continuous performance test.

ruled out here that these deficits are not related to

more basic deficits including working memory or
attention impairments although a recent study suggests
that deficits in the IGT in suicide attempters are largely
independent from them (Richard-Devantoy et al.
299 v. 281
156 v. 152
277 v. 252
190 v. 327
196 v. 244
244 v. 396
128 v. 209

2013b). In addition, we cannot assume that these defi-

cits affect all suicide attempters. For instance, one
n

study reported disadvantageous decision-making to

be mainly found in attempters who used violent
means (Jollant et al. 2005). This will have to be clarified.
Animals
Stroop

WCST
TMTB

However, we believe that these findings support at

Tests

CPT
FAS
IGT

the cognitive level the general model of vulnerability

 Neuropsychological markers of vulnerability to suicidal behavior 7
Table 3. Summary of findings
Neuropsychological tests
Alterations specifically related to suicidal behavior
IGT (net score)
Animals (number of words)
Greater alterations in suicidal behavior than in mood disorder
Stroop (time during interference)
Alterations specifically related to mood disorder
TMTB (time completion)
FAS (number of words)
WCST (perseverative errors)
CPT (commission errors)
IGT, Iowa gambling task; Animals, animal verbal fluency test; TMTB, trail-making test part B; FAS, FAS verbal fluency test;
WCST, Wisconsin card sorting test; CPT, continuous performance test.
* p < 0.05, ** p < 0.01, *** p < 0.001, (*) contrast became significant after excluding studies responsible for heterogeneity.
to suicidal behavior (Mann, 2003), with patients at
higher risk of suicide showing alterations not found
in patients at lower risk.
At the neurocognitive level, we could hypothesize
that vulnerability to suicidal acts results from a com-
bination of alterations in value-based/motivational/
reward-learning processes (supporting decision mak-
ing as measured by the IGT) on one side, and in cogni-
tive control processes (as measured by Animals
and Stroop) on the other side (Jollant et al. 2011).
Cognitive control refers to mechanisms that ‘orches-
trate thought and action in accordance with internal
goals’ (Miller & Cohen, 2001) and, therefore, encom-
pass multiple functions from task switching, response
inhibition, error detection, response conflict and work-
ing memory (Glascher et al. 2012). This schematic dis-
tinction is generally supported by neuroimaging and
lesion studies (Kouneiher et al. 2009; Stuss, 2011;
Glascher et al. 2012). In the case of suicide attempters,
disadvantageous IGT performance has been related
to deficient encoding of abstract risk in the ventro-
lateral orbitofrontal cortex (Jollant et al. 2010), a region
that was also more responsive to social signals of rejec-
tion in this population compared with patient controls
(Jollant et al. 2008). However, decreased verbal fluency
has been linked to more dorsal prefrontal regions,
including the anterior cingulate and the dorsolateral
prefrontal cortices (Audenaert et al. 2002; Oquendo
et al. 2003). These latter brain regions also underlie
brain processing during Stroop (Alvarez & Emory,
2006), although specific investigations of suicide
attempters are lacking.
A clinical translation of this neurocognitive model
could be that vulnerable individuals are more likely
to strongly value particular life events, notably social
Suicide attempters Suicide attempters Patient controls
v. patient controls v. healthy controls v. healthy controls
*** **
* ***
** *** **
** **
*** ***
** (*)
* (*)
signals of rejection, which, when they happen, lead
to an intense negative state. Their difficulty to control
this response (possibly associated with a ruminative
mode of thinking; O‘Connor & Noyce, 2008) and
with a pre-existing difficulty to envision the long-term
consequences of some options, may limit the extent
of their choices and lead them to consider suicide as
the only possible way to escape this painful state. An
additional hypothesis could be that limited verbal abil-
ities (as revealed by the animal verbal fluency test)
may reduce the possibilities to solve problems at an
explicit level and, consequently, increase the risk of
‘acting out’ negative emotions and suicidal ideas.
In addition, disadvantageous decision-making may
also increase the risk of interpersonal difficulties, a
classical trigger of suicidal crisis (Jollant et al. 2007).
This proposed model has yet to be properly tested in
empirical studies. Of note, this model (and the results
of this meta-analysis) partly overlaps with Mark
Williams’s ‘cry of pain’ cognitive model (Williams &
Pollock, 2001). This model proposed that vulnerable
people show: (1) a higher sensitivity to signals of
defeat as revealed by the emotional version of the
Stroop; (2) the feeling to be trapped associated with
lower problem-solving abilities and too general auto-
biographic memory; and (3) the feeling of hopelessness
correlated with reduced verbal fluency (using a modifi-
ed version). The link with the ‘escape from self’ theory
of suicide is less obvious (Baumeister, 1990).
The two other implications of our findings are
more speculative at this stage. The IGT, Animals and
Stroop could be helpful tests in the future for assessing
the long-term suicidal risk of patients with mood dis-
orders. These neuropsychological tests could be part
of a future comprehensive assessment of patients
8 S. Richard-Devantoy et al.

(a)
Study name Statistics for each study Sample size Hedges's g and 95% CI
Hedges's Standard Lower Upper Suicide Patient Relative
g error Variance limit limit Z-Value p-Value Attempters Controls weight
Jollant et al, 2005 -0.725 0.237 0.056 -1.191 -0.260 -3.054 0.002 69 25 13.81
Malloy-Diniz et al, 2009 -0.844 0.329 0.108 -1.489 -0.200 -2.567 0.010 18 21 7.49
Oldershaw et al, 2009 -0.107 0.251 0.063 -0.598 0.384 -0.428 0.669 54 22 12.51
Jollant et al, 2010 -0.927 0.409 0.167 -1.729 -0.126 -2.269 0.023 13 12 4.93
Martino et al, 2010 -0.520 0.249 0.062 -1.008 -0.033 -2.093 0.036 22 63 12.69
Gilbert et al, 2011 -0.431 0.248 0.061 -0.916 0.054 -1.741 0.082 28 39 12.78
Bridge et al, 2012 -0.600 0.226 0.051 -1.044 -0.156 -2.650 0.008 40 40 15.06
Legris et al, 2012 -0.326 0.329 0.109 -0.971 0.320 -0.989 0.323 29 13 7.47
Gorlyn et al, 2013 -0.113 0.243 0.059 -0.589 0.364 -0.463 0.643 26 46 13.25
-0.473 0.092 0.008 -0.654 -0.293 -5.142 0.000 299 281

-2.00 -1.00 0.00 1.00 2.00

Patient Controls Suicide Attempters

Results indicate that suicide attempters made significantly more risky than safe choices relative to patient controls.

(b)

Study name Statistics for each study Sample size Hedges's g and 95% CI

Hedges's Standard Lower Upper Suicide Patient Relative

g error Variance limit limit Z-Value p-Value Attempters Controls weight

Keilp et al, 2001 -0.400 0.285 0.081 -0.958 0.159 -1.403 0.161 29 21 19.39
Richard-Devantoy et al, 2012 -0.567 0.316 0.100 -1.187 0.053 -1.791 0.073 20 20 16.44
Keilp et al, 2013 -0.047 0.162 0.026 -0.364 0.270 -0.290 0.772 72 80 40.41
Richard-Devantoy et al, 2013a -0.550 0.248 0.062 -1.036 -0.063 -2.213 0.027 35 31 23.76
-0.320 0.143 0.020 -0.601 -0.040 -2.236 0.025 156 152

-2.00 -1.00 0.00 1.00 2.00

Patient Controls Suicide Attempters

Results indicate that suicide attempters named significantly fewer animals in 1 min than patient controls.

(c)

Study name Statistics for each study Sample size Hedges's g and 95% CI
Hedges's Standard Lower Upper Suicide Patient Relative
g error Variance limit limit Z-Value p-Value Attempters Controls weight
Becker et al, 1999 0.163 0.251 0.063 -0.329 0.656 0.649 0.516 31 31 13.80
Keilp et al, 2001 0.430 0.285 0.081 -0.129 0.989 1.507 0.132 29 21 12.12
Malloy-Diniz et al. 2009 0.282 0.316 0.100 -0.338 0.902 0.891 0.373 18 21 10.78
Cha et al, 2010 0.099 0.179 0.032 -0.253 0.451 0.551 0.582 68 56 18.04
Richard-Devantoy et al, 2011 1.955 0.528 0.279 0.920 2.990 3.701 0.000 10 10 5.22
Legris et al, 2012 0.016 0.327 0.107 -0.626 0.658 0.048 0.962 29 13 10.33
Richard-Devantoy et al, 2012 0.735 0.321 0.103 0.106 1.363 2.291 0.022 20 20 10.60
Keilp et al, 2013 0.354 0.163 0.027 0.035 0.673 2.173 0.030 72 80 19.11
0.372 0.135 0.018 0.108 0.636 2.762 0.006 277 252

-2.00 -1.00 0.00 1.00 2.00

Patient Controls Suicide Attempters

Results indicate that suicide attempters took significantly more time than patient controls in conditions of interference.

Fig. 1. Comparison of the Iowa gambling task net scores (a), animal verbal fluency scores (b) and Stroop interference scores
(c) between suicide attempters and patient controls. CI, Confidence interval.

with mood disorders. However, longitudinal studies or with a unipolar depressive disorder (Westheide
will be first necessary to measure the predictive et al. 2008), or a combination of patients with both sub-
value of these cognitive deficits versus the simple col- types of mood disorder (Jollant et al. 2005). Also, some
lection of clinical signs and symptoms and past history. studies were conducted in patients who were acutely
Finally, interventions aiming at remediating cognitive depressed (Abrahams et al. 2009; Richard-Devantoy
deficits revealed by these tests should be developed et al. 2012), while others focused on those in remission
and their overall clinical utility assessed. (Jollant et al. 2005). Also, participants in some studies
were on medication while in other studies they were
not. Moreover, it was not possible to separate neuro-
Limitations
psychological targets of low from high lethality suicide
First, studies included in this review examined various attempters, and violent and non-violent suicide
populations. For example, some enrolled only adoles- attempters, because too few studies distinguished
cents (Bridge et al. 2012), middle-aged (Keilp et al. both groups. Personality disorders were not formally
2013) or elderly (Richard-Devantoy et al. 2012) partici- assessed or reported in too many studies to be taken
pants. In addition, some studies included only patients in to account in analyses. Finally, some studies were
with bipolar depression (Malloy-Diniz et al. 2009), only conducted in males (Jollant et al. 2010) while
 Neuropsychological markers of vulnerability to suicidal behavior 9
most included both genders. Of note, the effect of
several variables (including the intensity of depressive
symptoms, age, gender, and the proportion of unipolar
and bipolar disorders) could be ruled out here. Meta-
analyses have often been criticized for combining
heterogeneous studies, for their potential of publi-
cation bias, and for the inclusion of poor-quality trials.
In the present study, however, these concerns were
addressed by the use of stringent inclusion criteria
and by the objective examination of both publication
bias and heterogeneity (see online Supplementary
material). Second, as our main focus was on suicide
attempters, contrast between non-suicidal patients
and healthy controls was only based on studies that
included a suicidal group. Consequently, many studies
have not been taken into account in this contrast.
Third, only patients with mood disorders have been
included in the analyses. Similar analyses should be
conducted in other clinical populations. Finally,
many tests and related functions could not be assessed,
as they had not been used in a sufficient number of
studies.
Conclusion
Performance at the IGT, animal category verbal fluency
test and Stroop test were found to be deficient in
patients with histories of suicidal acts in comparison
with patients with mood disorders but no suicidal
act history. These results shed light on possible mech-
anisms underlying the suicidal process. In addition,
these tests may become part of future systematic
assessment of the vulnerability to suicidal behavior
and guide therapeutic and preventative interventions.
Supplementary material
For supplementary material accompanying this paper
visit http://dx.doi.org/10.1017/S0033291713002304.
Acknowledgements
We thank Dr G. Turecki for his support and
Mrs Alexandra Hoehne for manuscript editing.
S.R.-D. received a post-doctoral grant from the
Canadian Institutes for Health Research (CIHR).
F.J. and M.B. received a ‘chercheur-boursier clinicien’
salary grant from the Fond de Recherche du
Québec – Santé (FRQS).
Declaration of Interest
None.
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