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Acta Psychiatr Scand 2005: 112: 294–301 Copyright  2005 Blackwell Munksgaard

All rights reserved ACTA PSYCHIATRICA


DOI: 10.1111/j.1600-0447.2005.00585.x
SCANDINAVICA

Executive functioning in depressed patients


with suicidal ideation
Marzuk PM, Hartwell N, Leon AC, Portera L. Executive functioning in P. M. Marzuk, N. Hartwell,
depressed patients with suicidal ideation. A. C. Leon, L. Portera
Acta Psychiatr Scand 2005: 112: 294–301.  2005 Blackwell Munksgaard. Department of Psychiatry, Weill Medical College,
Cornell University, New York, NY, USA
Objective: Suicidal thinking has been associated with cognitive
rigidity, however, not all depressed patients contemplate suicide.
Therefore, we hypothesized that compared with depressed subjects
without suicidal ideation, depressed individuals with suicidal ideation
would display poorer performance on measures of executive
functioning that involve mental flexibility.
Method: In-patients with a current major depressive episode who had
no current suicidal ideation (n ¼ 28) were compared with those who
had current suicidal ideation (n ¼ 25) on measures of executive Key words: cognition disorders; depression;
functioning and two neurocognitive tests that predominantly assess neuropsychological tests; frontal lobe; suicide
non-frontal regions. Peter M. Marzuk MD, Office of Curriculum and
Results: Compared with non-suicidal depressed patients, depressed Educational Development, Weill Medical College,
suicidal patients performed significantly worse on several measures of Cornell University, 1300 York Avenue, Box 243,
executive functioning after controlling for age, IQ, severity of New York, NY 10021, USA.
depression and prior suicide attempts. The two groups performed E-mail: pmmarzuk@med.cornell.edu
Presented in part at the 29th Annual Meeting of the
similarly on tests that predominantly assess non-frontal regions.
International Neuropsychological Society, Chicago, IL,
Conclusion: Depressed individuals contemplating suicide have February 14–17, 2001.
cognitive rigidity, which does not appear to be a global brain
dysfunction. Suicidal mental states may result from dysfunctional
executive decision-making that is associated with the frontal lobe. Accepted for publication May 26, 2005

Significant outcomes
• Compared with non-suicidal depressed patients, suicidal depressed patients performed significantly
worse on several measures of executive functioning after controlling for age, IQ, severity of
depression and history of prior attempts.
• The pattern of test results suggests a mental inflexibility associated with frontal lobe dysfunction may
underlie suicidal thinking and the Ôexecutive decisionÕ to commit suicide.
• Because both those depressed subjects with suicidal ideation and without suicidal ideation performed
similarly on neurocognitive tests that predominantly assess non-frontal brain regions, the cognitive
rigidity of suicidal ideation does not appear to be part of a global brain dysfunction.

Limitations
• Depressed individuals were not studied medication-free; however, the suicidal and non-suicidal
groups did not differ on the types of medications they were taking at the time of testing.
• Personality traits, which might correlate with some neuropsychological measures, were not assessed.
• The person who administered the neurocognitive tests was not blind to the subjectsÕ suicidal status.

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hypothesized that compared with non-suicidal


Introduction
depressed patients, depressed patients who had
Persons in suicidal mental states are often consid- suicidal ideation would also display poorer per-
ered to have cognitive rigidity, a broad term that formance on tests of executive functioning, partic-
includes dichotomous (all-or-none) thinking, and ularly tasks that require cognitive flexibility. To
problem solving deficits (1–5). Individuals with all- discount the possibility that poorer performance in
or-none thinking conceptualize their problems in the suicidal ideation group is merely part of a diffuse
absolute dichotomies such as Ôgood or badÕ, Ôright global brain dysfunction, we also administered two
or wrongÕ, Ônow or neverÕ, etc. Rigid adherence to tests that tap into functions that are primarily based
dichotomies can lead to lethal situations in which a in non-frontal regions. We hypothesized there
depressed, suicidal person sees his coping options would be no difference between the two groups on
in the all-or-none terms of a miserable life vs. these measures.
death, with few, if any, intermediate possibilities
between these stark choices. The cognitive rigidity
Aims of the study
of suicidal thinkers may also contribute to problem
solving deficits (6–12). That is, when cognitively The aim of the study was to determine whether,
rigid and depressed individuals are overwhelmed compared with depressed, non-suicidal individuals,
by stresses, they become incapable of generating depressed individuals with suicidal ideation display
alternative solutions necessary for adaptive coping decreased cognitive flexibility as measured by
and become increasingly hopeless. High levels of neuropsychological tests of executive functioning.
hopelessness then place these individuals at greater
risk for suicide.
The thought of ultimately committing suicide is, Material and methods
in effect, an Ôexecutive decisionÕ likely made, in
Subjects
part, in the prefrontal areas of the brain. These
brain regions involve the weighing of changing All subjects were recruited from the in-patient unit
alternatives and generating of new ones, the ability of the Payne Whitney Psychiatric Clinic of the New
to strategize out of Ôcorners, traps or dead endsÕ, York Presbyterian Hospital, a 64-bed unit of a
and the initiation and execution of plans – all private, university hospital. To be included in the
functions that are hampered by cognitive rigidity. study, subjects had to meet criteria for a current
Depression, the most common syndrome associ- major depressive episode (unipolar or bipolar) on
ated with suicidal thinking, and the most common the basis of the Structured Clinical Interview for
clinical syndrome associated with completed sui- DSM-IV (25), which was administered by a doc-
cide, is known to involve cognitive dysfunction, toral candidate in psychology (N.H.). In addition,
particularly on ÔexecutiveÕ tasks (13–18). In addi- subjects were required to be over 18 years of age,
tion, evidence from postmortem and neuroimaging primarily English speaking and capable of under-
studies suggest depression involves alterations in going structured clinical interviews and neuropsy-
the structure, metabolism or receptor binding of chological testing. Individuals were excluded from
the prefrontal cortex, especially the left dorsolat- study if they had mental retardation, dementia,
eral prefrontal region (19–22). However, most alcohol or substance abuse within the past
depressed patients do not commit suicide, and 6 months, or a history of anoxic or traumatic
many have never been suicidal ideators. Thus it is brain damage, cerebrovascular accidents, transient
important to identify the specific factors that ischemic attacks or loss of consciousness that
increase the risk of suicide in depressed individuals. exceeded 1 h.
Several studies (8, 23) including a recent, well As the study involved seriously depressed and
controlled one by Keilp et al. (24), have found that suicidal in-patients, it was not possible to withhold
depressed patients with a history of suicide attempts psychotropic medications prior to testing. However,
have more cognitive rigidity as evidenced by dimin- we excluded patients who were currently taking
ished performance in executive functioning com- lithium, conventional antipsychotics, tertiary amine
pared with depressed patients without a history of tricyclic antidepressants such as imipramine or
suicide attempts. Suicidal thinking is much more amitriptyline, or medications known to affect neu-
common than suicidal behavior, but it is not known rocognitive functioning (26). In addition, we exclu-
if the same relative decrease in executive perform- ded individuals who had received electroconvulsive
ance would be found in depressed suicidal ideators treatment in the past year. To assess the possibility
compared with depressed non-ideators. As cognitive of impaired performance caused by the sedating
rigidity is mainly a disturbance in thinking, we effects of psychotropic medications, we also exclu-

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ded subjects who were not able to repeat at least a situations, strategic planning, and set shifting.
five-digit sequence forward on the Wechsler Adult These included the Wisconsin Card Sorting Test
Intelligence Scale-Revised (WAIS-R) (27) Digit (WCST) (34, 35); the Mazes subtest of the Wechsler
Span Subtest. The study was approved by the Intelligence Scale for Children, Third Edition
institutional review board of the Weill Medical (WISC-III) (36); two measures of verbal and figural
College of Cornell University. After a complete fluency, the Controlled Oral Word Association Test
description of the study to the subjects, we obtained (COWAT) (37, 38) and the Five Point Test (FPT)
their written informed consent. (39) respectively; the Stroop Color Word Test
(SCWT) (40); and the Trail Making Test, Parts A
and B (41). For the latter we used difference score
Measures of suicidal ideation
(trails B minus A), which removes the psychomotor
All subjects received the Scale for Suicidal Ideation element from the test and yields a purer measure of
(SSI), which is a 19-item clinician-administered set shifting.
scale that assesses current levels of suicidal ideation To ensure that poorer performance in executive
(28). It has high internal consistency (coefficient tasks in suicidal subjects was not part of a more
alpha ¼ 0.90 in this sample) as well as satisfactory diffuse cognitive impairment, subjects were admin-
levels of concurrent, discriminate, and constructive istered two tasks that are not considered primary
validity. A maximum score of 38 may be obtained, measures of executive functioning. These included
indicating extreme levels of suicidality. Items 4 and the Boston Naming Test (BNT) (42), a confronta-
5 pertain to current suicidal thoughts of an active tion naming task that requires the subject to
or passive nature. They also serve as gate items, identify a series of 60 pictured objects and the
with a positive response on either one leading to Rey Osterieth Complex Figure Test (43) – Copy
inquiry into the remaining 14 items regarding Condition that requires a subject to copy a
details about current suicidal thoughts. The meas- complex geometric figure.
ure yields both categorical (yes or no – either item 4 All subjects received the neuropsychological bat-
or 5 > 0) and continuous (total score on all 19 tery within 7 days of admission to the psychiatric
items) variables, which were used in subsequent unit. Subjects were assessed between 10 a.m. and
statistical analyses. Individuals who scored >0 on 3 p.m. to minimize possible effects of diurnal vari-
either item 4 or 5 were considered to be currently ation in depressive symptoms. To account for
suicidal. Individuals who received a score of 0 for possible effects of fatigue related to the order of
both these items were considered to be currently test presentation, subjects were randomly assigned
non-suicidal. The suicidal status (i.e. current suici- by computer-generated random numbers to receive
dal ideation vs. no current suicidal ideation) was the tests in one of two possible sequences: i) WAIS-R
assessed with the SSI immediately prior to the Digit Span, AMNART, Trail Making Test (parts A
administration of the neuropsychological battery. and B), COWAT, FPT, SCWT, Rey Copy WCST,
In addition, subjects were asked about the number, WISC-III Mazes and BNT or ii) WAIS-R Digit
dates and circumstances of prior suicide attempts. Span, WCST, WISC-III Mazes, Rey Copy BNT,
AMNART, Trail Making Test (parts A and B),
COWAT, FPT, and SCWT. All neuropsychological
Neurocognitive and psychopathologic assessments
assessments were administered by a single examiner
Immediately prior to neuropsychological assess- (N.H.) who had had extensive prior experience in the
ment, all subjects were administered standard rating administration of neurocognitive tests.
scales to assess severity of depression, anxiety, and
hopelessness, and impulsivity. These scales included
Statistical analyses
the Hamilton Rating Scaling for Depression
(HRSD) (29), 24 items; the Hamilton Anxiety The demographic and clinical characteristics of
Scale HAS) (30), the Beck Hopelessness Scale suicidal and non-suicidal subjects were compared
(31), and the Barratt Impulsiveness Scale (BIS) using t-tests for continuous variables and chi-
(32). To obtain an estimate of verbal intelligence squared tests for categorical variables. The neuro-
(VIQ), which correlates with performance on many psychological performance of the suicidal and non-
executive measures, subjects received the American suicidal subjects was compared using a multiple
New Adult Reading Test (AMNART) (33). Sub- linear regression approach to analysis of covariance
jects underwent a neuropsychological battery that (ANCOVA). Age and VIQ skills are known to be
consisted of standardized measures of executive related to many cognitive test scores. In addition,
functioning, including mental flexibility, problem depression is associated with cognitive effects such
solving, ability to generate multiple solutions to as decreased attention, concentration, psychomotor

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speed, and memory. Thus, the separate regression (60% women, 60% Caucasians), with nearly half
models for each neuropsychological variable inclu- of them having at least some college education, and
ded two successive blocks of variables: i) age, VIQ, average VIQ. There were no significant differences
severity of depression, history of prior suicide on these demographic characteristics between the
attempts, and ii) suicide status (i.e. current ideation suicidal and non-suicidal groups with the minor
vs. no ideation). The hypothesized differences in exception of age (Table 1).
neuropsychological performance between the suici- Most of the study group (approximately 85%)
dal and non-suicidal groups were evaluated with an had a current major depression (unipolar). Nine-
F-test of the significance of the incremental propor- teen percent also had dysthymia. The suicidal and
tion of variance (R2 change) accounted for by suicide non-suicidal groups did not differ in type of
status, over and above that accounted for by age, depression (major depression vs. bipolar) nor in
VIQ, severity of depression and history of prior mean age of onset of depression (early 20s),
suicide attempts. The two-tailed alpha level for each number of previous depressive episodes (approxi-
test was set at 0.05. mately 6–7), length of current episode (10–
12 weeks) or proportion with a previous suicide
attempt (about 50%) (Table 1). In the group with
Results current suicidal ideation, seven of 25 (28%) had
made a recent suicide attempt (attempt within
Characteristics of the study groups
1 month of admission) compared with five of 28
The study group (n ¼ 53), as a whole, was com- (18%) in the group with no current suicidal
posed of persons with an average age of 40 years ideation (v2 ¼ 2.27, d.f. ¼ 2, P ¼ 0.32).

Table 1. Demographic and clinical characteristics of the study groups

Statistics
Current suicidal No current suicidal
Characteristics ideation (n ¼ 25) ideation (n ¼ 28) Test d.f. P-value

Demographics
Age, years – mean (SD) 36.0 (11.9) 42.3 (11.2) t ¼ 1.97 51 0.05
Female (%) 56.0 64.3 v2 ¼ 0.11 1 0.74
White (%) 56.0 67.9 v2 ¼ 3.89 3 0.27
Education £12 years (%) 64.0 42.9 v2 ¼ 2.55 2 0.28
Estimated verbal IQ – mean (SD)* 106.3 (7.2) 108.9 (8.5) t ¼ 1.18 51 0.25
Right-handed (%)  96.0 92.9 v2 ¼ 0.24 1 0.62
Diagnosesà(%)
Major depression 84.0 89.3 v2 ¼ 0.03 1 0.87
Bipolar disorder depressed 16.0 10.7 v2 ¼ 0.03 1 0.87
Dysthymia 16.0 21.4 v2 ¼ 0.02 1 0.88
Illness characteristics, mean (SD)
Age of onset of first MDE, (years) 22.8 (13.5) 23.5 (12.9) t ¼ 0.18 51 0.86
No. of depressive episodes 6.0 (4.3) 6.9 (3.6) t ¼ 0.86 51 0.39
Length of current episode, (weeks) 13.9 (22.1) 11.0 (13.5) t ¼ )0.57 51 0.57
Previous suicide attempt (%) 60.0 39.2 v2 ¼ 2.27 2 0.32
Psychopathologic Measures, mean (SD)
HRSD 22.4 € 3.8 21.7 € 6.0 t ¼ )0.52 51 0.61
HAS 10.2 € 2.8 10.1 € 2.8 t ¼ )0.13 51 0.90
BHS 11.8 € 4.6 8.1 € 5.6 t ¼ )2.61 51 0.01
BIS 52.1 € 18.8 48.3 € 18.0 t ¼ )0.74 51 0.46
Current medications
SSRI antidepressants§ 44.0 67.9 v2 ¼ 2.17 1 0.14
Benzodiazepines– 24.0 46.4 v2 ¼ 2.00 1 0.16
Antipsychotics** 16.0 21.4 v2 ¼ 0.02 1 0.88
Mood stabilizers   12.0 17.9 v2 ¼ 0.04 1 0.83

MDE, major depressive episode; HRSD, Hamilton Rating Scale for Depression (24-item version with suicide item removed from total score); HAS, Hamilton Anxiety Scale; BHS,
Beck Hopelessness Scale; BIS, Barratt Impulsiveness Scale.
*Assessed by American New Adult Reading Test.
 Assessed by direct observation.
àTotal may exceed 100% as those with major depression or bipolar disorder, depressed may also have dysthymia.
§Includes fluoxetine, paroxetine, and also venlafaxine.
–Includes alprazolam, diazepam, flurazepam, lorazepam, midozolam, oxazepam, quazepam, temazepam, triazolam.
**Includes risperidone, olanzapine.
  Includes divalproex sodium, valproic acid, carbamazepine.

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At the time of neuropsychological testing, both primarily assess non-frontal regions, i.e. the BNT
groups were moderately depressed (mean HRSD and the Rey Copy Task.
score <23) and had comparable levels of anxiety
and impulsivity. However, not unexpectedly, the
Discussion
group with current suicidal ideation was signifi-
cantly more hopeless (Table 1). In this study we found that compared with
Approximately one-half of the study group were depressed non-suicidal patients, patients who
taking selective serotonin reuptake inhibitors were depressed and had current suicidal ideation
(SSRI) antidepressants; one-third were taking displayed poorer performance on several measures
benzodiazepines, one-fifth were taking either ris- of executive functioning after controlling for age,
peridone or olanzapine, and one-seventh were estimated VIQ, and severity of depression. In these
taking a mood stabilizer. However, there were no variables, a substantial proportion of the variance
differences between the suicidal and non-suicidal (8–21%) was accounted for by current ideation
groups in the proportion of patients taking a status.
particular class of medication (Table 1). Although the pattern of specific neurocognitive
tests is somewhat different from that seen in other
studies of suicidal individuals, our findings are in
Neuropsychological performance
general accord with the concept of Ôexecutive
In ANCOVAs that controlled for age, VIQ and dysfunctionÕ associated with suicidality. For exam-
severity of depression, compared with non-suicidal ple, Bartfai et al. (8) found that compared with
depressed persons, the depressed persons with healthy men, or men with chronic pain syndromes,
suicidal ideation showed significantly worse per- male suicide attempters did significantly worse on
formance on several measures of executive func- verbal and design fluency tests, but showed no
tioning including the WCST (number of difference on the Uses of Objects Tests, WCST or
perseverative errors), trails B minus A, and the Mazes. Mark et al. (23) administered a modified
WISC-III mazes (Table 2). There were no group Stroop task (i.e. presentation of neutral or emo-
differences on verbal or figural fluency or the tional words) and found that compared with
Stroop Interference Task. As hypothesized, there controls, patients with suicide attempts showed
were no differences between suicidal and non- greater interference with emotional words related
suicidal groups in performance on measures that to overdose themes. Keilp et al. (24) found that

Table 2. Performance on neuropsychological measures

Statistics*
Current suicidal No current suicidal
Measures ideation (n ¼ 25) mean (SD) ideation (n ¼ 28) mean (SD) B  R2 R2 change F P-value

WCST
No. of perseverative errorsà 14.4 (6.5) 8.6 (2.7) 5.72 0.34 0.23 16.30 <0.001
Failures to maintain setà 0.56 (0.77) 0.36 (0.91) 0.18 0.04 0.01 0.48 0.49
TMT
B minus A (secs) à 43.5 (26.1) 27.8 (13.8) 14.5 0.19 0.10 5.70 0.02
WISC – III Mazes subtest
Raw score§ 21.0 (3.8) 23.0 (3.5) )2.22 0.12 0.08 4.02 0.05
Fluency
Verbal (COWAT) no. of words generated§ 39.0 (11.6) 45.5 (10.4) )3.90 0.23 0.03 1.60 0.21
Non-verbal (FPT) no. of designs generated§ 31.2 (8.5) 33.0 (7.7) )0.56 0.17 0.001 0.06 0.81
SCWT
Interference– )1.5 (7.2) 2.3 (5.5) )3.19 0.16 0.05 2.90 0.10
BNT
Raw score§ 52.4 (5.0) 53.3 (4.0) 0.25 0.33 0.0007 0.05 0.83
ROCFC
Raw score§ 34.5 (1.8) 35.1 (1.2) )0.62 0.16 0.04 2.08 0.16

WCST, Wisconsin Card Sorting Test; TMT, Trail Making Test; WISC-III, Wechsler Intelligence Scale Test–third edition; COWAT, Controlled Oral Word Association Test; FPT, Five
Point Test; SCWT, Stroop Color Word Test; BNT, Boston Naming Test; ROCFC, Rey Osterrieth Complex Figure Copy.
*ANCOVA controlling for age, verbal IQ, and severity of depression (HRSD score) and history of previous attempt; d.f. ¼ 1, 48.
 The regression coefficient that represents the covariate-adjusted difference between those with current suicidal ideation (x ¼ 1) with those without current suicidal ideation
(x ¼ 0).
àA higher number indicates poorer performance.
§A lower number indicates poorer performance.
–A negative number indicates poorer performance.

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attempters who made high lethal attempts could be plement those of postmortem studies which have
distinguished from those with a history of low also suggested that there are serotonergic and
lethal attempts, non-attempters, and non- alpha-adrenergic binding changes in the frontal
depressed comparison subjects on measures of cortices (in particular the ventrolateral prefrontal
verbal fluency, failure to maintain set on the cortex) of suicides compared with those of non-
WCST, and on total recall in the Buschke Selective suicidal controls. Postmortem studies of individ-
Reminding Test. uals who had committed suicide, in effect, come
In contrast, Ellis et al. (44) found no difference closest to ÔcapturingÕ an individual’s brain state at
on neuropsychological functioning of patients who the time of suicide, i.e. presumably when he or she
had recently attempted suicide and those with no was thinking of suicide. The poorer performance
history of attempts. With the exception of an of our suicidal subjects is probably not part of a
interactive effect of age and group (recent attempt- diffuse, global brain dysfunction as suicidal sub-
ers vs. non-attempters), King et al. (45) found jects performed nearly identically as non-suicidal
virtually no differences among elderly depressed in- subjects on measures that are predominantly Ônon-
patients on a range of neuropsychological tasks. In frontalÕ, i.e. the BNT and the Rey Copy Condi-
both these studies however, suicide status was tion.
based on a history of suicide attempts and current Studies of past attempters and non-attempters
suicidal ideation was not assessed. It is possible would seem to suggest that performance differences
that following an attempt many patients are no in neurocognitive functioning are either traits or at
longer acutely suicidal. In our study we based least long-lasting cognitive ÔstylesÕ, as these studies
suicide status on the presence of current suicidal assessed the neurocognitive function of attempters
ideation and controlled for a history of prior weeks or even months after the individual’s
suicide attempts. We believe cognitive rigidity is attempts. These studies did not refer to current
more likely to be reflected in current thinking, i.e. a suicidal ideation at the time of testing. Our study
suicidal mental state, than in past attempts, no design does not permit us to assess conclusively
matter how recent. whether the cognitive rigidity that we observed in
Our results, taken together with those of other the suicide ideators is a state phenomenon or a
studies, suggest that a mental inflexibility may trait. However, it should be noted that our two
underlie suicidal thinking and the Ôexecutive decis- groups of ideators and non-ideators had about
ionÕ to commit suicide. Both the WCST and trails equal numbers of persons with past suicide
B minus A tasks assess a subject’s ability to shift attempts. Thus, our finding of group differences
cognitive set and to change a response pattern among current ideators and current non-ideators
based on environmental cues and contingencies. suggests that the cognitive rigidity may be tempor-
Likewise, poor performance on the Mazes subtest ary and not a persistent characteristic or cognitive
of the WISC-III suggests a cognitive rigidity that style in some individuals. Moreover, Perrah and
involves a failure to develop appropriate strategies Wichman (46) found no differences in executive
within time limits. Although our group compari- measures that assess cognitive flexibility and set
sons for verbal fluency were not statistically shifting between past attempters and non-attempt-
significant, the directionality of the finding (suici- ers. Past attempters were also less rigid than recent
dal subjects had poorer performance) together with attempters of other studies (47). Longitudinal
the Bartfai et al. (8) and Keilp et al. (24) studies, studies in which neuropsychological functioning
suggest suicidal subjects may have difficulty gener- can be assessed repetitively in different stages of the
ating alternative solutions to problems. Likewise, illness and studies of high-risk relatives are needed
the directionality of our findings on Stroop Inter- to resolve whether cognitive rigidity of suicidal
ference (suicidal subjects had poorer performance), thinkers is a state, trait, or even a ÔscarÕ that follows
along with the findings of Mark et al. (23), suggest the initial attempt.
that suicidal subjects may have difficulties in Several limitations warrant comment. We did
shifting perceptual set given changing demands not measure personality traits or assess personality
and may also have poor inhibitory control. Acutely disorders that influence cognitive style and there-
suicidal individuals appear to lack the cognitive fore might correlate with some neuropsychological
flexibility needed to generate new solutions or shift measures. However, the suicidal and non-suicidal
among alternative strategies. In effect, they become groups did not differ on a measure of impulsive-
ÔstuckÕ on suicide or to use Shneidman’s (1) more ness. For ethical reasons we could not test severely
poetic term, have a Ôtunnel visionÕ. depressed suicidal individuals off medications;
Neurocognitive evidence of diminished execu- however, it should be noted that the suicidal and
tive functioning among suicidal individuals com- non-suicidal group did not differ on the type of

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Marzuk et al.

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