INECO Frontal Screening: An Instrument To Assess Executive Dysfunction in Schizophrenia
INECO Frontal Screening: An Instrument To Assess Executive Dysfunction in Schizophrenia
Abstract. Although several brief sensitive screening tools are available to detect executive dysfunction, few have been
developed to quickly assess executive functioning. The INECO Frontal Screening (IFS) is a brief tool which has proved
be useful for the assessment of the executive functions in patients with dementia. The aim of this study was to explore
whether the IFS is as sensitive and specific as the BADS, a battery designed to assess the dysexecutive syndrome,
in schizophrenia. Our sample comprised a group of 34 schizophrenic patients (Mean age = 39.59, DP = 10.697) and 31
healthy controls (Mean age = 35.52, DP = 10.211). To all groups were administered the BADS, Wisconsin Card Sorting Test
and IFS. The results suggest that schizophrenic patients performed significantly worse than the control group in all tests
(p < .05). The IFS total score was 13.29 for the experimental group and 26.21 for the control group (p < .001). Considering
a cut-off of 14 points, the IFS sensitivity was 100% and specificity 56% in detection of executive dysfunction in schizo-
phrenia, compared with the BADS, that if we consider a cut-off of 11 points, was a sensitivity of 100% and a specificity
of 50%. Thus, IFS is a brief, sensitive and specific tool for the detection of executive dysfunction in schizophrenia.
Within the scope of study of schizophrenia, cognitive medial / hippocampus temporal lobe (Graham et al.,
dysfunction has received the main focus of attention 2009), basal ganglia (Eslinger & Grattan, 1993) and
in many recent investigations, being associated with a thalamus (Tanibuchi & Goldman-Rakic, 2003).
wide range of deficits, including impairment of memory, The impairment of executive functions can further
attention, executive functioning and general intellectual cause an impact on functional results in patients with
functioning (Goldberg, David, & Gold, 2003). schizophrenia, which can have a variety of effects on
The impairment of executive functions is one of the the daily life activities of these patients, including the
more important and central deficits that is associated capability to work or go to school, responsibilities
with schizophrenia (Carter et al., 2011; Goldman-Rakic, at home or engaging in appropriate social relation-
1994; Kerns, Nuechterlein, Braver, & Barch, 2008; ships (Freedman & Brown, 2011; Kerns et al., 2008).
Liddle & Morris, 1991; Reeder, Newton, Frangou, & Additionally, Green, Kern, and Heaton (2004) discovered
Wykes, 2004), occurring not only in the chronic stage that the executive function deficits found in patients
of the disease, but also in the first episode (Chan, with schizophrenia determined the poor functional
Chen, & Law, 2006), in the prodromic stage (Cornblatt, results with regards to living in the community, self-
Lenzenweger, Dworkin, & Erlenmeyer-Kimling, 1992; care activities, social problem solving capabilities and
Davidson et al., 1999), and in direct descendants (Snitz, psychosocial competences.
Macdonald, & Carter, 2006; Szöke et al., 2005). In this manner, if we try to understand the nature of
On the other hand, a large research body has iden- the difficulties inherent to executive dysfunction, they
tified a strong association between executive deficits can be reasonably understood as being a failure at the
and structural and functional cerebral deficits, by which level of Norman & Shallice’s SAS model (1986), also
the executive processes, although strongly dependant creating the basis for the main characteristics of dysex-
on the frontal cortex (Eisenberg & Berman, 2010), also ecutive syndrome, a term proposed by Baddeley (1986),
require the cooperation of external structures of the characterized as a more functional cognitive deficit asso-
frontal lobes, namely the inferior parietal lobe (Jansma, ciated with frontal lobe syndrome. SAS is interpreted
Ramsey, van der Wee, & Kahn, 2004; Jonides et al., 1998), as being necessary for the effective control of an action
in a number of situations: situations requiring plan-
Correspondence concerning this article should be addressed
ning or decision making; situations which involve the
to Tânia S. Silva. Instituto Superior de Ciências da Saúde - Norte.
Rua Central de Gandra, 1317. 4585–116. Gandra (Portugal).
correction of errors or problem solving, situations in
Phone: +351–224157100/+351–224157102. which the replies are not well perceived or contain new
E-mail: tanya_sylva@live.com.pt sequences of actions; situations deemed dangerous
2 T. Silva et al.
or technically difficult and, finally, situations which On the other hand, instruments designed specifically
demand overcoming a strong usual response. Various to quickly assess executive functions are few. Thus, a
tests have been planned based on the SAS model and screening tool that is easy to use denotes high sensi-
have been designed specifically for the acquisition of tivity, specificity and predictive value would be of
different SAS components, namely the Six Element great importance to practitioners. Various instruments
Test, first described by Shallice and Burgess (1991), later of cognitive screening have desirable diagnostic and
incorporated into BADS (Wilson, Alderman, Burgess, statistical properties (Keefe et al., 2004), but few were
Emslie, & Evans, 1996), and also the Hayling Test developed to specifically assess executive functioning.
(Burgess & Shallice, 1996), incorporated into INECO As proof of the intrinsic difficulties that arise with the
Frontal Screening. development of such tools, various screening batteries
Nonetheless, the neuropsychological study of execu- that have tried to measure executive dysfunction do
tive dysfunction and its corresponding rehabilita- not show reasonable psychometric characteristics.
tion, however, face inherent difficulties. One of them For example, Rothlind and Brandt (1993) proposed a
is the precise and valid evaluation of executive func- brief cognitive screening test for the identification of
tions. Executive functions are developed to under- frontal-subcortical dysfunction, however, patients with
stand a variety of competences in order to achieve a AD showed worse results in this test than patients
goal (Damasio, 1995; Shallice, 1988; Stuss et al., 2005; with frontal dysfunction, demonstrating the low spec-
Stuss & Benson, 1986). Therefore, a failure in tests ificity of the tool. Royall, Mahurin and Gray (1992)
which assess executive functions may be due to many developed an interview for executive functioning by
reasons, such as damage in any process of its compo- reflecting on a problem, however, it also revealed itself
nents is difficult to be completely overlooked after the to be sensitive to non-executive dysfunction. Ettlin
emergence of cerebral lesions or psychopathologies. and Kischka (1999) developed the Frontal Lobe Index,
Furthermore, the neuropsychological evaluation devices but application of this tool requires at least 40 minutes.
which have been used for this purpose are of an exces- Nonetheless, this difficulty is not unilateral, in other
sively artificial and structured nature and thus, few words, a solely psychometric problem, but also an
are those that have been developed to assess execu- executive functioning construct which is multifaceted,
tive functions quickly, not reflecting conveniently complex and dynamic. Thus, even though efforts have
the demands of real life, where dysfunctions are felt been made to measure executive functions, their com-
(Barbosa & Monteiro, 2008). plexity constitutes an enormous challenge (Miyake
To this end new instruments have emerged that et al., 2000).
combine a solid theoretical foundation with adequate Given the above mentioned difficulties and based on
psychometric and ecologic al validity. The Behavioral previous research relating to executive testing (Clark,
Assessment of the Dysexecutive Syndrome (BADS) is Manes, Antoun, Sahakian, & Robbins, 2003; Clark &
one of the instruments that systematically use everyday Manes 2004; Manes et al., 2002; Torralva et al., 2007), a
tasks as a way to assess executive functions (Wilson tool has recently been developed at the Institute of
et al., 1996). This battery was developed in response to Cognitive Neurology (INECO) in Buenos Aires, which
the need for more sensitive, valid and reliable neu- aims at diagnosing executive dysfunction in a quick
ropsychological instruments in this area, while at the and specific manner: the INECO Frontal Screening
same time, trying to overcome the deficiencies asso- (IFS; Torralva, Roca, Gleichgerrcht, López, & Manes,
ciated with conventional tests. Despite its relatively 2009). The authors of this study designed this screening
recent development, according to several researchers test in order to make available to health care providers
(Crawford, 1998; Groth-Marnat, 2000; Norris & Tate, a sensitive and specific test, for early diagnosis of fron-
2000; Wilson, Evans, Emslie, Alderman, & Burgess, tal dysfunction in dementia patients. To achieve this,
1998), this battery shows a promising potential for they applied IFS to patients with Alzheimer’s Disease
responding to the aforementioned needs. (AD) and Frontotemporal Dementia (FTD). The results
This battery has also been applied to the research of showed that patients with FTD presented more serious
executive functioning in schizophrenia. The research executive dysfunction, represented by their lower score
of Evans, Chua, McKennna, and Wilson (1997) and in the general IFS, in comparison with patients with
Krabbendam, Vugt, Derix, and Jolles (1999) showed AD. In this manner, the study of Torralva et al. (2009)
that BADS is an essential contributor in the identifi- showed that IFS is a quick, sensitive and specific tool
cation of executive deficits in people diagnosed with for the diagnosis of executive dysfunction associated
schizophrenia, especially in those with their general with neurodegenerative diseases.
intellectual capability intact. Nonetheless, it is as exten- In this manner, the aim of the present study is to
sive exam that requires time to be applied, expensive verify if the INECO Frontal Screening, test which
equipment or highly trained professionals to apply it. quickly assesses executive functions, is as sensitive
Ineco Frontal Screening 3
and specific as BADS, a battery for assessment of dys- includes four questions that assess the capability to
executive syndrome with high ecological validity, for foresee or estimate how long it takes, in average, to
detecting executive dysfunction in schizophrenia. complete various tasks, events or daily activities. The
Zoo Map Test assesses the planning of actions. And
Method lastly, the Modified Six Elements Test is a test of a planning,
temporal organization of tasks and self-assessment of
Participants
success test (Wilson et al., 1996).
65 Individuals participated in this research, in which
the experimental group consisted of 34 patients with Wisconsin Card Sorting Test
schizophrenia, mainly males (70.6%), with ages ranging
Consists in matching 128 answer cards with four
between 22 and 62 years (M = 39.59, DP = 10.697). Data
stimulus cards. While carrying out the task, the par-
collection was obtained from the Alto Ave Hospital
ticipants try to lay out the cards according to a criterion
Center, E.P.E., in Guimarães, whose board and ethics
which is unknown to them and should be inferred by
committee consented to this research being carried out.
means of feedback from the test administrator. The total
Candidate selection was carried out based on inclusion
number of errors, perseverative and non-perseverative
and exclusion criteria for the sample, having included
errors and the number of complete categories was
candidates with confirmed diagnosis of Schizophrenia,
considered for the purpose of score. This test assesses
according to the criteria established in the DSM-IV-TR,
capabilities for planning, organized research, orien-
and excluding all uncompensated candidates from a
tated behavior and the adequate use of feedback to
psychopathological point of view at the time of data
change strategies and modulate an impulsive response
collection, with dual diagnosis, with organic cerebral
(Strauss, Sherman, & Spreen, 2006).
lesions, who presented a severe level of cognitive deteri-
oration or even mental deficiency, who were illiterate,
INECO Frontal Screening
due to the nature of the proposed tasks, and that pre-
sented a current or recent history of substance abuse. Is a brief, sensitive and specific neuropsychological
On the other hand, the control group consisted in 31 exam to detect executive dysfunction in neurode-
individuals, mainly males (61.3%), with ages ranging generative pathologies, developed by Torralva et al.
between 20 and 55 years (M = 35.52, DP = 10.211). This (2009) and adapted for the Portuguese population by
group was recruited in the Vale do Sousa residential Caldeira (2011). The exam consists of eight sub-tests.
area, in order to guarantee the best possible adjust- In the Motor Programming subtest the subject should
ment of the samples with regards to school qualifica- perform the Luria series “fist, edge, palm” by initially
tions (obligatory education or less), or socioeconomic copying the administrator, and by subsequently doing
background (lower or lower-middle class). All par- the series on his or her own then by repeating the
ticipants were informed of the nature and aims of the series six times alone. In the Conflicting Instructions
study and participation in all neuropsychological tests (Sensitivity to Interference) subtest, the subjects are
was voluntary. asked to hit the table once when the administrator hits
The two groups do not differ significantly with it twice, or to hit the table twice when the adminis-
regards to gender t(63) = –.783, p = .437, age t(63) = 1.566, trator hits it only once. In the Go–No Go subtest, the
p = .122, or level of education t(63) = –.856, p = .395. subjects are told that when the test administrator hits
the table once, they should hit it once as well, but when
Materials the examiner hits twice, they should do nothing. In the
Backward Digit Span subtest, the subjects are invited
In order to assess the executive functioning of the par-
to repeat string of digits in the reverse order. In turn,
ticipants, neuropsychological tests deemed pertinent
in the Verbal Working Memory subtest, the subjects are
to completing the objectives of the study were applied:
asked to list the months of the year backward, start-
BADS, WCST and INECO Frontal Screening.
ing with December. In the Spatial Working Memory
subtest, the administrator presents the subject with
Behavioral Assessment of the Dysexecutive Syndrome
four cubes and points at them in a given sequence,
Consists of six tasks. For each task a reference score is which the patient should repeat in reverse order. In the
obtained (maximum of 4 and minimum of 0). The Rule Abstraction Capacity - Proverb Interpretation subtest,
Shift Card test assesses the capability of changing an three proverbs are read to the subjects who are then
established response pattern using familiar items. The invited to explain their meaning. The Verbal Inhibitory
Action Program assesses the capability of solving prac- Control subtest is inspired in the Hayling Test, which
tical problems. Key Search is a test to assess the capa- measures the capacity of the subject to inhibit an
bility to plan a strategy. The Temporal Judgment Test expected response (Torralva et al., 2009).
4 T. Silva et al.
The Mini Mental State Examination (MMSE; Folstein, Analysis and Data Processing
Folstein, & McHugh, 1975)
The statistical analysis was performed using the sta-
It was also applied as a control method, in the sense tistical analysis program SPSS – Statistical Package for
of excluding all individuals who presented a score the Social Sciences, version 19.0. Univariate descrip-
lower than 22 points (cognitive deficit cut-off score tive analysis procedures were employed, specifically
for the Portuguese population with 1 to 11 years of central tendency and dispersion measures (median
education). and standard deviation) and frequency distribution.
Subsequently, a bivariate descriptive analysis using
Procedures Student’s t-test for independent samples was applied.
The neuropsychological assessment was made in the Differences with p < .05 were considered as signifi-
Psychiatric and Mental Health Department of the cant. The ability of the IFS to assessment executive
Alto Ave Hospital Center, in Guimarães. The hospi- functions in comparison to BADS was determined
tal’s ethics committee issued a favorable report for using a receiver operating characteristic (ROC) curve
completion of the study and the informed consent analysis.
was obtained from all individuals that taking part in
the study. Before the executive functioning evalua- Results
tion, all participants were submitted to a MMSE, with Description of the executive functioning of the
the aim of determining the existence of more sever Experimental and Control Group
neurocognitive disorders. Consecutively, the previously
mentioned neuropsychological tests were applied, such The results obtained by the two groups in the BADS,
as BADS, WCST and IFS, with the aim of obtaining the regarding to total score obtained, demonstrate that the
results of the executive functioning evaluation. The schizophrenia group obtained results which were
instruments used in this study were applied trans- clearly lower (M = 10.65, DP = 3.074) in comparison
versely, with a duration that varied between one or with the control group (M = 20.55, DP = 1.786), being
two sessions, each lasting an hour, depending on the the difference highly significant, t(54)= –16.046, p < .001,
performance of the individual and also to avoid pos- 95% CI [–11.163, –5.664] (see Figure 1). Also, the time
sible effects of fatigue. All participants completed the it took to complete the battery revealed a statistically
proposed assessment. significant difference, t(52) = 9.019, p < .001, 95% CI
Figure 1. Averages and standard error of the total score obtained by the Experimental and Control Groups in BADS
completion.
Ineco Frontal Screening 5
[135.182, 212.534], in favor of the control group In turn, if we analyze the scores obtained for each sub-
(M = 183.61, DP = 53.889) which demonstrated itself test, we can conclude the group of patients with schizo-
quicker in comparison with the experimental group phrenia clearly presents inferior results to those of the
(M = 357.47, DP = 97.213) (see Figure 2). control group in all IFS subtests in a manner which is
With regards to the scores obtained in each BADS statistically significant (see Table 4).
subtest, we can realize that the schizophrenia group
was less successful than the control group in all the Definition of sensitivity and specificity of IFS
subscales of the battery, without exception (see Table 1). comparatively to BADS
The performance differences revealed to be statistically
The capacity of IFS in briefly assessing executive func-
significant in all the subtests (p < .05).With regards to
tioning, in comparison to BADS, was determined by
the time spent for complete each task, for the subtests
the analysis of the ROC curves (see Figure 3). Analysis
in which time was a factor (subtests 1, 2, 3 and 5), it
of the ROC curve for the total IFS score between the
could be verified that the schizophrenia group required
control group and the patients with schizophrenia gen-
significantly longer periods of time in comparison with
erated an area under ROC curve of .999. If we consider
the control group, in order to conclude the tasks of all
a cut-off point of 14 points, IFS shows 100% sensitivity
the subscales (see Table 2).
and 56% specificity, in the distinction between the
In regard to performance in the WCST, the group
patients with schizophrenia and control group. In turn,
of patients with schizophrenia presented a greater
the ROC curve analysis for the total BADS score gener-
number of errors, as well as a greater number of per-
ated an area under curve of 1. If we consider a cut-off
severative errors, more perseverative answers, more
point of 11 points, BADS shows a 100% sensitivity and
non-perseverative errors and a lesser amount of com-
50% specificity. This way, we can verify that IFS pro-
pleted categories in comparison to the control group,
duces sensitivity and specificity results very close to
in a statistically significant manner (see Table 3)
those of BADS when detecting executive dysfunction
Finally, the total scores obtained by the different
in schizophrenia.
groups in the INECO Frontal Screening allow us under-
stand that the group of patients with schizophrenia was
Discussion
less successful (M = 13.29, DP = 4.859), in a highly signif-
icant manner, t(44) = –14.291, p < .001, 95% CI [–14.737, The current research revealed the existence of deficits
–11.094], than the control group (M =26.21, DP = 1.948). in executive functions of patients with schizophrenia,
Figure 2. Averages and standard error of the total time spent (in seconds) by the Experimental and Control Groups in the
completion of the BADS subscales.
6 T. Silva et al.
Table 1. Averages, Standard Deviations, t Values, p Values and Confidence Intervals of the results of the Experimental and Control Groups
in each of the BADS subtest
Experimental Control
Group Group 95% CI
BADS Subscales M SD M SD t p LL UL
Rule Shift 2.18 1.167 3.81 .402 –7.662 < .001 –2.059 –1.2
Action Program 2.41 1.184 3.52 .570 –4.858 < .001 –1.561 –.647
Key Search 1.15 1.077 2.68 1.137 –5.573 < .001 –2.079 –.982
Temporal Judgement 1.38 .739 2.81 .833 –7.301 < .001 –1.814 –1.034
Zoo Map 1.26 .864 3.74 .445 –14.720 < .001 –2.815 –2.139
Modified Six Elements 2.15 .657 3.97 .180 –15.524 < .001 –2.058 –1.583
Table 2. Averages, Standard Deviations, t Values, p Values and Confidence Intervals of time spent (in seconds) by the Experimental and
Control Groups in completing each of the BADS subtest
Experimental Control
Group Group 95% CI
Rule Shift 51.76 14.317 27.26 6.846 8.925 < .001 18.986 30.027
Action Program 138.59 52.977 66.68 8.972 7.793 < .001 53.180 90.642
Key Search 61.74 31.581 32.29 18.932 4.604 < .001 16.628 42.262
Zoo Map 105.38 45.824 57.39 38.100 4.606 < .001 26.993 68.998
Table 3. Averages, Standard Deviations, t Values, p Values and Confidence Intervals of the results obtained by the Experimental and Control
Groups in the various dimensions of the WCST
Experimental Control
Group Group 95% CI
WCST measure M SD M SD t p LL UL
Total errors 61.00 15.510 25.52 12.720 10.028 < .001 28.413 42.555
Perseverative errors 37.94 15.510 15.35 7.209 7.078 < .001 16.161 29.012
Perseverative responses 41.18 18.610 16.97 8.420 6.855 < .001 17.103 31.314
Non-perseverative errors 23.06 12.507 10.19 7.499 5.080 < .001 7.789 17.941
Categories completed 2.76 1.372 5.74 .514 –11.778 < .001 –3.487 –2.467
corroborating the data found in the literature in these patients to use feedback in order to control
(Eisenberg & Berman, 2010; Everett, Lavoie, Gagnon, & or modify their behavior (Strauss et al., 2006). In turn,
Gosselin, 2001; Heinrichs & Zakzanis, 1998; Palmer, the Action Program Test requires the subjects to be
Heiby, Fujii, & Kameoka, 2008). Analysing the results, capable to manipulate a variety of materials in order
the poor performance of the schizophrenia group in to solve a non-routine problem (Wilson et al., 1996),
completing BADS suggests impairment in multiple and its validity lies in the difficulty found by patients
components of executive functioning, since it is not a with pre-frontal lesions to develop new plans or cog-
one-dimensional construct (Miyake et al., 2000). In the nitive strategies in order to solve a problem. This test
Rule Shift Card subtest, we can verify some difficulty implies the action of the Supervisory Attentional System
Ineco Frontal Screening 7
Table 4. Averages, Standard Deviations, t Values, p Values and Confidence Intervals of the results obtained by the Experimental and Control
Groups in each of the INECO Frontal Screening subtests
Experimental Control
Group Group 95% CI
IFS subtests M SD M SD t p LL UL
Motor programming 1.32 1.224 2.97 .180 –7.742 < .001 –2.076 –1.213
Conflicting instructions 2.18 1,114 2.84 .374 –3.271 .002 –1.071 –.253
Go–No go 1.97 1.218 2.90 .301 –4.322 < .001 –1.370 –.496
Backwards Digit Span 1.94 .884 2.90 .301 –9,466 < .001 –2.884 –1.879
Verbal Working Memory 1.38 .817 2.00 .000 –4.408 < .001 –.903 –.333
Spatial Working Memory 1.21 .845 2.84 .898 –7,552 < .001 –2,065 –1,201
Proverb interpretation .38 .551 2.34 .907 –10.385 < .001 –2.335 –1.578
Verbal inhibitory control 2.91 2,165 5.97 .180 –8.198 < .001 –3.814 –2.298
(Modified Hayling test)
Figure 3. ROC curve analysis for evaluation of specificity and sensitivity of IFS comparatively to BADS in order to detect
executive dysfunction in schizophrenia.
(Norman & Shallice, 1986), which stimulates or inhibits the tube in order to access the plug, for example. Our
the representation of actions which are normally acti- research shows that the process of the Supervisory
vated by certain stimuli, avoiding the creation of rou- Attentional System is compromised in the schizo-
tine actions, such as completing the test by inverting phrenia group since they showed less capacity to solve
8 T. Silva et al.
the presented problem. In the Key Search Test, the In turn, with regards to the performance of the
patients with schizophrenia demonstrated poor per- groups in completing the INECO Frontal Screening,
formance, evidencing difficulties in planning efficient it can be concluded that the group of patients with
actions and in their capacity to monitor their own per- schizophrenia clearly presents poorer results in compar-
formance, since the patients could look at the lines ison to the control group. Similar results were obtained
drawn to show the itinerary followed and come to in a study by Báez et al. (2011), in which two groups of
the conclusion that the search was not efficient. On adult patients with Bipolar Disorder and with Attention
the other hand, in the Temporal Judgment Test, it is Deficit Hyperactive Disorder obtained significantly
required of the subject to make an estimate of the time lower scores than the control group with regards to
needed to complete various tasks, therefore the exis- the total score obtained in IFS. In this manner, this
tence of a highly significant difference between the screening test proved to be a solid and useful tool for
groups in this test could be attributed to the impair- the detection of executive dysfunction in various psy-
ment of abstract judgment and thought capacity of the chiatric disorders, both in the study of Báez et al. (2011)
schizophrenic patients, since the answers are based as in the current study.
on common sense. In the Zoo Map Test, the schizo- Thus, the results obtained by means of the neu-
phrenia group also demonstrated a less significant ropsychological tests used in the current study dem-
capacity for planning when compared to the control onstrate the impairment of various executive function
group. In this test, the subjects have to identify and components in the group with schizophrenia, revealing
temporarily organize various stages, depending on the presence of an executive dysfunction. This disor-
the rules and specific objectives. The deficit demon- der relates to a clinical state characterized by disor-
strated by the schizophrenia group may be related to der in the planning and organization of actions, poor
the frequent errors made by the patients with frontal capacity for initiative, perseverance, inflexibility, a
lesions when they try to follow specific instructions. difficulty in conceiving and implementing strategies,
This becomes obvious in the labyrinth tests, or in difficulty in problem solving and in selective attention
learning tasks, where the subject has to choose the (Goldberg, David, & Gold, 2003; Palmer & Heaton,
most adequate answer from between a set of answers 2000). In the cases of pathology, lesion or cerebral
to achieve the final objective. Finally, in the Modified dysfunction, the dysexecutive syndrome may mani-
Six Elements Test, the schizophrenia patients dem- fest itself through a myriad of problems in everyday
onstrated difficulties in the conception and implemen- life, namely inappropriate social behavior, difficulty
tation of strategies, since the task requires the capacity with decision making, high levels of impulsiveness,
to manage time. distraction, difficulty in using feedback from the envi-
These results are consistent with the findings obtained ronment to regulate behavior, preventing full func-
in other scientific investigations, such as the studies of tional recovery and the possibility of reclaiming a
Evans et al. (1997), Ihara, Berrios, and McKenna (2000), socially responsible life, independent and well adjusted
Krabbendam et al. (1999). (Barbosa & Monteiro, 2008; Gioia, Isquith, Guy, &
The group of patients with schizophrenia demon- Kenworthy, 2000).
strated a poorer performance in the WCST when com- In turn, when analyzing the objectives of this study,
pared to the control group, which is consistent with the it was possible to verify that IFS is as sensitive and
conclusions found in literature (Heinrichs & Zakzanis, specific as BADS. It is an assessment battery for dys-
1998). According to Koren et al. (1998), perseveration executive syndrome with high ecological validity, par-
and the total number of categories completed seem ticularly efficient in the detection of subtle difficulties
to translate the more sensitive scores into deficits in with the planning and organization of actions, espe-
schizophrenia; in fact, in the current study, significant dif- cially in cases of people for whom cognitive capacity
ferences were verified between controls and the schizo- seems to be preserved in well-structured situations
phrenics for the segment of perseverative answers (Strauss et al., 2006). In this way, the current study
and a poor performance in average of the patients concluded that IFS shows high sensitivity and spec-
with schizophrenia the level of number of categories ificity in comparison with BADS in the detection of
completed. According to Greve, Stickle, Love, Bianchini, executive dysfunction in schizophrenia, demonstrating
and Stanford (2005), these results demonstrate the dif- itself to be a good way to briefly assess functions related
ficulty of the patient in changing to correct principled with the frontal lobe, allowing for the differentiation
organization and as a consequence generate a large of the two groups included in the study.
number of perseverative answers and few completed To this end, the current study demonstrated that
categories. Thus, the performance of patients with IFS is an instrument of quick application and pos-
schizophrenia reflects a difficulty on abstraction and sesses high sensitivity in order to be used in clinical
cognitive flexibility level. practice. However, it is possible that by being as
Ineco Frontal Screening 9
sensitive as BADS, it is qualitatively less rich due to Burgess P. W., & Shallice T. (1996). Bizarre responses, rule
its lengthier nature and artificiality of the tasks, detection and frontal lobe lesions. Cortex, 32, 241–259.
since BADS is a robust exam, with good theoretical http://dx.doi.org/10.1016/S0010-9452(96)80049-9
Caldeira M. J. (2011). Adaptation and validation of INECO
background, good psychometric properties and has
Frontal Screening (Master’s Thesis). Instituto Superior de
good ecological validity, reflecting the everyday prob-
Ciências da Saúde – Norte: Gandra, Portugal.
lems of executive dysfunction presented by the patients.
Carter C. S., Barch D. M., Bullmore E., Breiling J.,
Yet, a brief cognitive screening tool which is easy to Buchanan R. W., Butler P., … Wykes T. (2011). Cognitive
apply and presents high sensitivity, specificity and pre- neuroscience treatment research to improve cognition in
dictive value such as IFS would be of great importance schizophrenia II: Developing imaging biomarkers to
to health care professionals since in clinical practice, enhance treatment development for schizophrenia and
they do not always have access to highly trained neu- related disorders. Biological Psychiatry, 70, 7–12.
ropsychologists, specific instruments to assess certain http://dx.doi.org/10.1016/j.biopsych.2011.01.041
cognitive domains or the length of time required to Chan R. C., Chen E. Y., & Law C. W. (2006). Specific
executive dysfunction in patients with first-episode
administer a complete neuropsychological battery.
medication-naïve schizophrenia. Schizophrenia Research,
With the advent of discoveries related to executive
82, 51–64. http://dx.doi.org/10.1016/j.schres.2005.
functioning and the implication of the frontal lobe in
09.020
such specific tasks, it is our understanding that this Clark L., & Manes F. (2004). Social and emotional decision-
exam is a very useful tool for health care professionals making following frontal lobe injury. Neurocase, 10,
for it allows them to evaluate certain areas of executive 398–403. http://dx.doi.org/10.1080/13554790490882799
functioning and providing information on the need to Clark L., Manes F., Antoun N., Sahakian B. J., &
carry out further neuropsychological exploration. It is Robbins T. W. (2003). The contributions of lesion laterality
definitely of vital importance to be able to count on and lesion volume to decision-making impairment following
sensitive and specific tools for the diagnosis of neu- frontal lobe damage. Neuropsychologia, 41, 1474–1183.
rological and psychiatric diseases with the aim of fur- http://dx.doi.org/10.1016/S0028-3932(03)00081-2
Cornblatt B. A., Lenzenweger M. F., Dworkin R. H., &
thering neuropsychological research and elaborate
Erlenmeyer-Kimling L. (1992). Childhood attentional
strategies for cognitive intervention in such a manner
dysfunction predicts social isolation in adults at risk
that the patients recover those capabilities that allow a for schizophrenia. The British Journal of Psychiatry, 161,
person to live in an independent manner, with a spe- 59–68.
cific goal, with self-sufficient behavior and in a satis- Crawford J. (1998). Introduction to the assessment of
factory way (Lezak, Howieson, & Loring, 2004). attention and executive function. Journal of Neuropsychological
Still, many additional limitations of this study may Rehabilitation, 8, 209–211. http://dx.doi.org/10.1080/
be observed. There is no current symptomatology 713755574
data for the patients, the sample is heterogeneous, Damasio A. R. (1995). Toward a neurobiology of emotion
the number of participants is relatively small and per- and feeling: Operational concepts and hypotheses. The
Neuroscientist, 1, 19–25. http://dx.doi.org/10.1177/
formance in the executive functioning tests and its
107385849500100104
relation to other cognitive processes may be different
Davidson M., Reichenberg A., Rabinowitz J., Weiser M.,
for individuals with schizophrenia that are stable in Kaplan Z., & Mark M. (1999). Behavioral and intellectual
comparison to those with more active and severe symp- markers for schizophrenia in apparently healthy male
toms. Further, future investigations should also explore adolescents. The American Journal of Psychiatry, 156,
behavioral observations (e.g., time taken to complete 1328–1335.
the tasks, latency of response, etc.) during IFS evalua- Eisenberg D. P., & Berman K. F. (2010). Executive function,
tion as alternative and complementary tools. neural circuitry, and genetic mechanisms in schizophrenia.
Neuropsychopharmacology, 35, 258–277. http://dx.doi.org/
References 10.1038/npp.2009.111
Eslinger P. J., & Grattan L. M. (1993). Frontal lobe and
Baddeley A. D. (1986). Working memory. Oxford, UK: frontal-striatal substrates for different forms of human
Clarendon Press. cognitive flexibility. Neuropsychologia, 31, 17–28.
Báez S., Gleichgerrcht E., Urquina H., Lischinsky A., Roca M., http://dx.doi.org/10.1016/0028-3932(93)90077-D
Manes F., & Torralva T. (2011, May). Utility of the INECO Ettlin T., & Kischka U. (1999). Bedside frontal lobe testing.
Frontal Screening (IFS) for the detection of executive The “frontal lobe score”. In B. L. Miller, & J. L. Cummings
dysfunction in patients with adult ADHD and bipolar (Eds.), The human frontal lobes. New York, NY: The Guilford
disorder. Paper presented at the Third International Congress on Press.
ADHD: From Childhood to Adult Disease. Berlin, Germany. Evans J. J., Chua S. E., McKenna P. J., & Wilson B. A.
Barbosa M., & Monteiro L. (2008). Recurrent criminal (1997). Assessment of the dysexecutive syndrome in
behavior and executive dysfunction. The Spanish Journal of schizophrenia. Psychological Medicine, 27, 635–646.
Psychology, 11, 259–265. http://dx.doi.org/10.1017/S0033291797004790
10 T. Silva et al.
Everett J., Lavoie K., Gagnon J., & Gosselin N. (2001). of cognition in schizophrenia: Reliability, sensitivity,
Performance of patients with schizophrenia on the and comparison with a standard neurocognitive battery.
Wisconsin Card Sorting Test (WCST). Journal of Psychiatry Schizophrenia Research, 68, 283–297. http://dx.doi.org/
and Neuroscience, 26, 123–130. 10.1016/j.schres.2003.09.011
Folstein M. F., Folstein S. E., & McHugh P. R. (1975). Kerns J. G., Nuechterlein K. H., Braver T. S., & Barch D. M.
Mini-mental State: A practical method for grading the (2008). Executive functioning component mechanisms
cognitive state of patients for the clinician. Journal of and schizophrenia. Biological Psychiatry, 64, 26–33.
Psychiatric Research, 12, 189–198. http://dx.doi.org/ http://dx.doi.org/10.1016/j.biopsych.2008.04.027
10.1016/0022-3956(75)90026-6 Koren D., Seidman L. J., Harrison R. H., Lyons M. J.,
Freedman D., & Brown A. (2011). The developmental course Kremem W. S., Caplan B., … Tsuang M. T. (1998). Factor
of executive functioning in schizophrenia. International structure of the Wisconsin Card Sorting Test: Dimensions
Journal of Developmental Neuroscience, 23 , 237–243. of deficit in schizophrenia. Neuropsychology, 12, 289–302.
http://dx.doi.org/10.1016/j.ijdevneu.2010.11.003 http://dx.doi.org/10.1037//0894-4105.12.2.289
Gioia G. A., Isquith P. K., Guy S. C., & Kenworthy L. Krabbendam L., Vugt E., Derix M., & Jolles J. (1999). The
(2000). BRIEF: Behavior rating inventory of executive function Behavioral Assessment of the Dysexecutive Syndrome as a
professional manual. Lutz, FL: PAR. tool to assess executive functions in Schizophrenia. The
Goldberg T. E., David A., & Gold J. M. (2003). Neurocognitive Clinical Neuropsychologist, 13, 370–375. http://dx.doi.org/
deficits in schizophrenia. In S. R. Hirsch, & D. R. Weinberger 10.1076/clin.13.3.370.1739
(Eds.), Schizophrenia (pp. 168–184). Oxford, UK: Blackwell Lezak M. D., Howieson D. B., & Loring D. W. (2004).
Science. Neuropsychological assessment (4th Ed.). New York, NY:
Goldman-Rakic P. S. (1994). Working memory dysfunction Oxford University Press.
in schizophrenia. The Journal of Neuropsychiatry and Clinical Liddle P. F., & Morris D. L. (1991). Schizophrenic symptoms
Neurosciences, 6, 348–357. and frontal lobe performance. The British Journal of
Graham S., Phua E., Soon C. S., Oh T., Au C., Shuter B., … Psychiatry, 158, 340–345. http://dx.doi.org/10.1192/
Yeh I. B. (2009). Role of medial cortical, hippocampal and bjp.158.3.340
striatal interactions during cognitive set-shifting. Manes F., Sahakian B., Clark L., Rogers R., Antoun N.,
NeuroImage, 45, 1359–1367. http://dx.doi.org/10.1016/j. Aitken M., & Robbins T. (2002). Decision-making
neuroimage.2008.12.040 processes following damage to the prefrontal cortex. Brain,
Green M. F., Kern R. S., & Heaton R. K. (2004). 125, 624–639. http://dx.doi.org/10.1093/brain/awf049
Longitudinal studies of cognition and functional Miyake A., Friedman N. P., Emerson M. J., Witzki A. H.,
outcome in schizophrenia: Implications for MATRICS. Howerter A., & Wager T. D. (2000). The unity and
Schizophrenia Research, 72, 41–51. http://dx.doi.org/ diversity of executive functions and their contributions to
10.1016/j.schres.2004.09.009 complex “Frontal Lobe” tasks: A latency variable analysis.
Greve K. W., Stickle T. R., Love J. M., Bianchini K. J., & Cognitive Psychology, 41, 49–100. http://dx.doi.org/10.1006/
Stanford M. S. (2005). Latent structure of the Wisconsin cogp.1999.0734
Card Sorting Test: A confirmatory factor analytic study. Norman D. A., & Shallice T. (1986). Attention to action:
Archives of Clinical Neuropsychology, 20, 355–364. Willed and automatic control of behavior. In R. I. Davidson,
http://dx.doi.org/10.1016/j.acn.2004.09.004 G. E. Schwartz, & D. Shapiro (Eds.), Consciousness and
Groth-Marnat G. (2000). Neuropsychological assessment in self−regulation: Advances in research and theory. New York, NY:
clinical practice: A guide to test interpretation and integration. Plenum Press.
Hoboken, NJ: Wiley. Norris G., & Tate R. (2000). The Behavioral Assessment
Heinrichs R. W., & Zakzanis K. K. (1998). Neurocognitive of the Dysexecutive Syndrome (BADS): Ecological,
deficit in schizophrenia: A quantitative review of the concurrent and construct validity. Neuropsychological
evidence. Neuropsychology, 12, 426–445. http://dx.doi.org/ Rehabilitation, 10, 33–45. http://dx.doi.org/10.1080/
10.1037//0894-4105.12.3.426 096020100389282
Ihara H., Berrios G. E., & McKenna P. J. (2000). Palmer B. W., & Heaton R. K. (2000). Executive dysfunction
Dysexecutive syndrome in schizophrenia: A cross-cultural in schizophrenia. In T. Sharma & P. D. Harvey (Eds.),
comparison between Japanese and British patients. Cognition in schizophrenia: Impairments, importance and
Behavioral Neurology, 12, 209–220. treatment strategies (pp. 51–72). New York, NY: Oxford
Jansma J. M., Ramsey N. F., van der Wee N., & Kahn R. S. University Press.
(2004).Working memory capacity in schizophrenia: Palmer C., Heiby E., Fujii D., & Kameoka V. (2008).
A parametric fMRI study. Schizophrenia Research, 68, Executive functioning in schizophrenia: The contributions
159–171. http://dx.doi.org/10.1016/S0920-9964(03) of attention, working memory, processing speed, and
00127-0 general intelligence. Graduate Student Journal of Psychology,
Jonides J., Schumacher E. H., Smith E. E., Koeppe R. A., 10, 38–45.
Awh E., Reuter-Lorenz P. A., … Willis, C. (1998). The role Reeder C., Newton E., Frangou S., & Wykes T. (2004). Which
of parietal cortex in verbal working memory. The Journal of executive skills should we target to affect social functioning
Neuroscience, 18, 5026–5034. and symptom change? A study of a cognitive remediation
Keefe R., Goldberg T. E., Harvey P. D., Gold J. M., therapy program. Schizophrenia Bulletin, 30, 87–100.
Poe M. P., & Coughenour L. (2004). The brief assessment http://dx.doi.org/10.1093/oxfordjournals.schbul.a007070
Ineco Frontal Screening 11
Rothlind J. C., & Brandt J. (1993). A brief assessment of Szöke A., Schurhoff F., Mathieu F., Meart A., Ionescu S., &
frontal and subcortical functions in dementia. Journal of Lebover M. (2005). Tests of executive functions in first-
Neuropsychiatry and Clinical Neurosciences, 5, 73–77. degree relatives of schizophrenic patients: A meta-analysis.
Royall D. R., Mahurin R. K., & Gray K. F. (1992). Bedside Psychological Medicine, 35, 771–782. http://dx.doi.org/
assessment of executive cognitive impairment: The 10.1017/S0033291704003460
executive interview. Journal of American Geriatrics Society, Tanibuchi I., & Goldman-Rakic P. S. (2003). Dissociation
40, 1221–1226. of spatial-, object-, and sound-coding neurons in the
Shallice T. (1988). From neuropsychology to mental structure. mediodorsal nucleus of the primate thalamus. Journal of
Cambridge, UK: Cambridge University Press. Neurophysiology, 89, 1067–1077. http://dx.doi.org/
Shallice T., & Burgess P. W. (1991). Deficits in strategy 10.1152/jn.00207.2002
application following frontal lobe damage in man. Torralva T., Kipps C. M., Hodges J. R., Clark L.,
Brain, 114, 727–741. http://dx.doi.org/10.1093/brain/ Bekinschtein T., Roca M., … Manes, F. (2007). The
114.2.727 relationship between affective decision-making and theory
Snitz B. E., Macdonald A. W., & Carter C. S. (2006). of mind in the frontal variant of frontotemporaldementia.
Cognitive deficits in unaffected first-degree relatives of Neuropsychologia, 45, 342–349. http://dx.doi.org/10.1016/
schizophrenia patients: A meta-analytic review of putative j.neuropsychologia.2006.05.031
endophenotypes. Schizophrenia Bulletin, 32, 179–194. Torralva T., Roca M., Gleichgerrcht E., López P., & Manes F.
http://dx.doi.org/10.1093/schbul/sbi048 (2009). INECO Frontal Screening (IFS): A brief, sensitive,
Strauss E., Sherman E., & Spreen O. (2006). A compendium and specific tool to assess executive functions in dementia.
of neuropsychological tests: Administration, norms and Journal of the International Neuropsychological Society, 15,
commentary. (3rd Ed.). Oxford, UK: Oxford University 777–786. http://dx.doi.org/10.1017/S1355617709990415
Press. Wilson B. A., Alderman N., Burgess P. W., Emslie H. E., &
Stuss D. T., Alexander M. P., Shallice T., Picton T. W., Evans J. J., (1996). Behavioral assessment of the dysexecutive
Binns M. A., Macdonald R., … Katz D. I. (2005). syndrome. Suffolk, UK: Thames Valley Test Company.
Multiple frontal systems controlling response speed. Wilson B. A., Evans J. J., Emslie H., Alderman N., &
Neuropsychologia, 43, 396–417. http://dx.doi.org/ Burgess P. (1998). The development of an ecologically
10.1016/j.neuropsychologia.2004.06.010 valid test for assessing patients with a dysexecutive
Stuss D. T., & Benson D. F. (1986). The frontal lobes. New York, syndrome. Neuropsychological Rehabilitation, 8, 213–228.
NY: Raven Press. http://dx.doi.org/10.1080/713755570