Brain Injury

ISSN: 0269-9052 (Print) 1362-301X (Online) Journal homepage: http://www.tandfonline.com/loi/ibij20

Attentional control and slowness of information

processing after severe traumatic brain injury

Marcos Ros, Jos A. Periez & Juan M. Muoz-Cspedes

To cite this article: Marcos Ros, Jos A. Periez & Juan M. Muoz-Cspedes (2004) Attentional
control and slowness of information processing after severe traumatic brain injury, Brain Injury,
18:3, 257-272, DOI: 10.1080/02699050310001617442

To link to this article: http://dx.doi.org/10.1080/02699050310001617442

Published online: 03 Jul 2009.

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 BRAIN INJURY, VOL. 18, NO. 3 (MARCH 2004), 257272

Attentional control and slowness of information

processing after severe traumatic brain injury

M A R C O S R I O S y}, J O S E A . P E R I A N E Z z
a n d J U A N M . M U N O Z - C E S P E D E S }
yDepartment of Basic Psychology II, Universidad Nacional de Educacion a Distancia
(UNED), Madrid, Spain
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zDepartment of Psychology, Universitat de les Illes Balears (UIB),

Palma de Mallorca, Spain
}Brain Damage Unit, Beata Mara Ana Hospital (HHSCJ), Madrid, Spain
Department of Basic Psychology II, Universidad Complutense (UCM), Madrid, Spain
(Received 29 April 2003; accepted 20 June 2003)

Attention is a basic cognitive function and a prerequisite for other cognitive processes and is frequently
impaired after traumatic brain injury. In the present study, 29 severe traumatic brain injury patients and
30 control subjects completed a battery of three neuropsychological tests of attention (WCST, TMT,
Stroop). The aim was to clarify the attentional mechanisms underlying tests performance and to
explore the types of attentional impairment after severe traumatic brain injury. Significant differences
were found between the control and clinical groups in almost all measures. However, some of these
differences disappeared when the speed of information processing was controlled using covariance
analysis. In addition, a factor analysis revealed a four-factor solution explaining 89.6% of the variance
in the data, i.e. cognitive flexibility, speed of processing, interference and working memory. This result
supports the view of at least four different subprocesses of attentional control underlie test per-
formance and allows one to differentiate between high- and low-level processes. The implications
for neuropsychological assessment and rehabilitation are discussed.

Introduction
Disorders of attention are a major problem after traumatic brain injury (TBI) that
produce deficits in other cognitive functions and in everyday activities. These
deficits are identified by care givers and family members as the most common
problems [13] likely to interfere with other cognitive functions, the rehabilitation
process, and predict difficulties in daily living activities and in the possibility of
return to work [4, 5]. Moreover, TBI patients and their families often complain
of memory and learning problems, but sometimes an exhaustive evaluation shows
that these deficits could be attributable to an attentional dysfunction or simply to
the slowness in the processing speed of cerebral systems.
Attention has been considered a complex and non-unitary process. Functional
neuroimaging and neuropsychological assessment have depicted theoretical models

Correspondence to: Marcos Ros Lago, Departmento de Psicologa Basica II, Facultad de
Psicologa UNED, C/ Juan del Rosal, 10, E-28040 Madrid, Spain. e-mail: mrios@psi.uned.es
Brain Injury ISSN 02699052 print/ISSN 1362301X online # 2004 Taylor & Francis Ltd
http://www.tandf.co.uk/journals
DOI: 10.1080/02699050310001617442
 258 M. Ros et al.

that have established that there may be cortical regions specific to the processes
required for an accurate attentional performance. In particular, the frontal lobes
and their complex connections with a wide range of cortical and subcortical struc-
tures (thalamus, brainstem, etc.) are considered to play a key role in information
processing [2, 6]. Some authors have suggested that separate but interrelated
brain circuits control attentional functions in humans [7, 8]. For example, cognitive
functions like task switching, interference control, error detection, allocation of
attentional resources, target selection and conflict resolution have been linked
to the executive network, which is supposed to be located in the anterior areas
of the brain, including the anterior cingulate gyrus and supplementary motor
areas [9, 10].
Despite the effort of researchers to offer a clear map of cognitive functions
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and their related brain regions, clinical evidence does not always support these
theoretical views. For example, in a recent study, patients with focal frontal injuries
did not differ from those with injuries beyond the frontal lobes in a battery address-
ing deficits in the supervisory attentional system (SAS) [11]. This finding has been
explained by some authors in terms of diffuse axonal injury [12, 13]. Owing to this
subcortical injury, apparently intact areas could not receive the appropriate input,
which explains the analogous deficits. On the other hand, white matter injury could
account for delayed reaction times by requiring a more diversified processing route
between stimulus and response, thus affecting test scores mediated by speed.
The neuropathology of TBI shows a common pattern of physiological abnor-
malities and structural changes. The most typical damage is often produced within
the frontal poles and the anterior areas of the temporal lobes in addition to diffuse
axonal injury [14, 15]. These patients suffer not only from localized damage in
a restricted area, but also of white matter injury in the cerebral hemispheres,
corpus callosum and frequently in the brainstem. The result is a poor attentional
performance typically associated with frontal dysfunction [1618].
An important challenge for researchers investigating the effects of TBI is the
identification of underlying cognitive mechanisms influencing or modulating
the impaired performance of this group of patients. These processes have been
studied from different points of view. The failure in attentional processes may be
due to a primary attentional control deficit or might be secondary to the impaired
processing speed. Some authors considered that these attentional deficits are a result
of the slowness of information processing (slowed processing hypothesis) [1922],
others that they are a consequence of a limited general processing resource
(attentional resource hypothesis) [23]. Furthermore, another group focused on
different aspects of the attentional processes, as sustained [24, 25], selective or
divided attention [26, 27], and looked for specific deficits of each component in
the attentional system (component process hypothesis).
Mental slowness implies that the amount of information processed per unit
of time is reduced. The slowness of information processing is one of the most
consistent findings in TBI patients and has been repeatedly demonstrated in this
population. Some investigators have suggested that TBI patients do not have specific
attention deficits but that they have characteristically slower, less precise functioning
of perceptual, motor and cognitive subroutines. There have been several lines
of evidence identified that support the slowed processing hypothesis [6, 19, 2830].
It has also been shown that speed of information processing contributes to memory
functioning (encoding), verbal comprehension and the capacity to cope with new
 Attentional control and slowness of information processing after severe TBI 259

situations. For this reason, it is believed that processing speed is a basic mechanism
that must be preserved for the correct functioning of other cognitive processes.
Attention may be considered a general processing resource and relevant to a
great variety of cognitive tasks. The authors who propose the conceptualization of
attention as a capacity-limited processing resource argued that some of the cognitive
deficits of patients with TBI may occur because they have less attentional resources
to allocate to task performances following injury [23].
Another group of studies has provided information about deficits in the specific
components of the attentional system [26, 31, 32]. Authors who defend this point
of view [33, 34] have argued against the hypothesis that the attentional deficits are
attributable to a general slowness factor. For them, the inability to perform two tasks
simultaneously becomes a specific deficit, presumably due to a failure in the central
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executive stage where decisions are made and responses coordinated.

From a methodological point of view, some authors have developed theoretical
concepts based upon the symptoms of attentional difficulty reported or observed
in individuals with TBI [35]. Others have proposed various models of attention
based on patterns of psychometric test scores. A common approach in research
on construct validity is to apply factor analytical methods to explore underlying
mechanisms of attention [36]. Exploratory principal component analysis (PCA) has
been used to examine the internal structure underlying neuropsychological batteries
postulating that each factor represents an independent cognitive dimension. Table 1
illustrates the lack of consensus between the models with regard to the selected
samples, the tests used to assess attentional processes, and the components of the
attentional function considered.
Recently, it has been suggested that concepts of attention can be reduced to two
underlying aspects: speed and control [38]. However, the presence of a deficit in
attentional control is a question that has not been completely answered thus far. It
is not known if attentional control is an unitary process or divided into dissociable
processes. For example, in a group of severe TBI patients there were no deficits
found in some central executive aspects of attention (such as planning, inhibition or
divided attention), with the exception of cognitive flexibility measured with the
Trail Making Test [39].
The following interpretations are still open to debate:
. Most of the studies demonstrating specific deficits in one of the attention
subprocesses used tasks the subject had to perform under time pressure.
There exists the possibility that experimental designs could be confusing
speed of processing with other aspects of attention; some deficits may simply
reflect a general slowness of information processing which would be most
evident when the task difficulty increases.
. There is a lack of consistency concerning the existence of deficits in
attentional control or its components in TBI patients. As noted above, the
few studies reporting impaired selective or divided attention deficits in this
population are inconclusive.
. Main reason for this discrepancy may be related to the concepts and choice
of tasks used to operationalize these hypothetical constructs, and specifically
the selection of test scores included as variables in the data analysis.
In view of these conclusions, the major goal of the present study was to identify
the cognitive mechanisms underlying attentional processes measured with three
 Table 1. Factor analysis studies of attention

260
Reference Sample Instruments Factors
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Mirsky et al. (1991) [59] two samples, WAIS, Cancelation Task, . focus, execute
n 203 neurological, WCST, Stroop Test, . shift
psychiatric and TMT, and CPT . sustain
healthy controls; . encode
n 435 healthy children
Boone et al. (1998) [58] one sample, WAIS, Rey Complex figure, . cognitive flexibility
n 250 neurological FAS, WMS, WCST, . speeded processing
and psychiatric Stroop Test, and ACT . basic/divided attention
patients and healthy and short-term memory
controls
Koren et al. (1998) [37] three samples, WCST . perseveration
n 292 schizophrenia; . failure to maintain set
n 91 relatives of . idiosyncratic sorting
schizophrenic patients;
n 141 normal controls
Pineda et al. (2000) [56] one sample, FAS, WCST, Stroop, . organization/flexibility
n 100 healthy and TMT . speed of information
young adults processing
. inhibitory control
. verbal fluency
Spikman et al. (2001) [38] two samples, Stroop, Reaction Time in . control
n 60 healthy controls; Distraction task, PASAT, . speed of reaction
n 60 TBI patients Reaction Time in Dual task,
TMT, Loc Score, and PERSREL
Bate et al. (2001) [80] two samples, TEA, Stroop, SDMT, . visual selective attention
n 35 TBI patients; WMS-R Digit Span, . attentional switching

M. Ros et al.
n 35 healthy controls Ruff 2s and 7s Selective . sustained attention
Attention Test, and PASAT . divided attention
Greve et al. (2002) [57] one sample, WCST . cognitive flexibility
n 68 TBI patients . problem-solving
. response maintenance
 Attentional control and slowness of information processing after severe TBI 261

instruments commonly used in clinical practice. The knowledge of these mecha-

nisms, their different components, and their relation to the properties involved in
the functioning of the systemanatomical substrates and lesions after TBIwill
enable us to learn more about the nature of these processes and the system where
they are implemented. From a clinical point of view, the identification of such
mechanisms and their dysfunctions is important because this information could
promote improved cognitive remediation programmes for TBI patients and also
it will help to develop more valid theoretical frameworks linking brain functions
and behaviour [23, 40].
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Methods
Participants
Data were obtained from 151 adults studied in the Brain Damage Unit at Beata
Maria Ana Hospital, Madrid. The sample included patients with brain injury (n 99)
as well as healthy controls recruited as volunteers for this study (n 52). Only a part
of this larger group was selected for the study according to the exclusion criteria.

Exclusion criteria
It has been demonstrated that age is highly influential on information processing
speed [41]. In order to assure that no age effects interfered with the final results, the
age criteria for participating in the study were limited to between 15 and 50 years.
In the patient group, only subjects with all the measures needed for the study
were included in the final sample. Patients with impairment that could interfere
with testing (such as visual difficulties, aphasia or apraxia) were excluded. All
patients were out of post-traumatic amnesia (PTA) at the time of testing according
Galveston Orientation and Amnesia Test (GOAT) criteria [42].
In the control group medical complications, psychiatric disturbance, substance
abuse or neurological disease were criteria for exclusion. All participants had normal
or corrected to normal visual acuity.
In agreement with the exclusion criteria, 29 patients with TBI were selected
from the original sample. All patients had a severe TBI as defined by a score of 8 or
less on the Glasgow Coma Scale (GCS) (mean 4.89; SD 1.34; range 37), with
the exception of two cases where GCS was not provided. In these latter cases, the
inclusion was based on information provided by the discharge report. PTA duration
score was also recorded. The mean PTA duration was 46 days (SD 31.88; range
299 days). For patients with more than 3 months in PTA, a score of 99 was
recorded. The mean age of the patient group was 28.69 years (SD 7.4; range
1648 years). The mean educational level for the group was 14 years (SD 3.6;
range 818 years). The mean time since injury was 12.07 months (SD 7.37; range
224 months).
Thirty healthy subjects were carefully matched for age and years of education to
the patients. The mean age of the control group was 25.82 years (SD 3.49; range
2235 years). The mean educational level was 15.71 years (SD 2.23; range 1419
years). In fact, the comparison of the groups according to both variables does not
yielded significant differences.
 262 M. Ros et al.

Instruments and procedures

Each participant completed a battery of neuropsychological tests as part of the usual
protocol employed at the Brain Damage Unit, administered by a staff neuro-
psychologist. Instructions for each test were presented verbally in all cases. Three
neuropsychological tests were selected to measure aspects of the attentional
processes: Trail Making Test (TMT) [43], Wisconsin Card Sorting Test (WCST)
[4446], and Stroop Test [47, 48].
In the TMT, the time (s) taken to complete each part was recorded. A derived
TMT score was calculated. The TMT A and TMT B ratio (B/A) provides an index
of the executive component of attention. Comparisons between Parts A and B
provide a measure of the executive control involved in managing performance
of two alternating tasks. This score reflects the additional cognitive control needed
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to complete Part B successfully. Some authors have supported the use of this ratio
in clinical practice, assuming that ratios > 3 points to executive difficulty, particular
for set-switching impairment [49].
In the present study, a standardized version of the WCST was used. Only the
percentages of correct responses, errors, perseverative responses, non-perseverative
errors and perseverative errors were included in the analysis.
For the Stroop Test, the number of correct responses in a fixed time of 45 s was
recorded for the colour (c), word (w), and colour-word (cw) subtests. A derived
score called interference was also obtained. This score gives an index on the capacity
to inhibit the prepotent response. The formula for the calculation of this score is:
CW
CW0 interference, where CW0 C  W=C W:
The descriptions of these tests are available in Lezak [50] as well as Spreen and
Strauss [51]. All participants gave written informed consent once the procedures had
been fully explained. Informed consent followed the guidelines of the institutional
ethics committee.

Statistical analysis
The data were analysed in two steps. First, a principal component analysis (PCA),
useful for descriptive purposes, was performed to examine the factor structure
among the three tests administered to normal control subjects and TBI patients.
In the second part, Students t- and MannWhitney U-tests were applied to deter-
mine differences between the groups in each of the test variables. Covariance
analyses were then used to control the influence of speed of information processing
and of other cognitive variables. All analyses were performed using SPSS v10.0
software (1999; SPSS, Inc., Chicago, IL, USA).

Results
Factor analysis
Twelve scores from the control subjects and patients were submitted to a PCA with
an orthogonal (varimax) rotation in order to explore the internal structure of the
battery.
A four-factor solution accounting for 89.6% of the variance was produced
(table 2). The significance loading criteria used was 0.40 [52]. WCST scores
(excluding the percentage of non-perseverative errors) and TMT B and TMT
 Attentional control and slowness of information processing after severe TBI 263

Table 2. Varimax-rotated component loadings from a principal component analysis on 12 scores of attention

Factors

1 2 3 4

WPE 0.957
0.174
0.111

WPR 0.950
0.161
0.109
WER 0.912
0.264
0.117 0.287
WCR
0.912 0.264 0.117
0.288
TMT B/A 0.630
0.242
0.187
0.509
STRW
0.225 0.906
0.142
STRC
0.219 0.873
TMT A
0.790
0.119 0.306
TMT B 0.485
0.761
0.217
0.144
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STRCW
0.304 0.715 0.580

STRI
0.178 0.980
WNPE 0.218
0.261 0.845

WPE, WCST Perseverative Errors; WPR, WCST Perseverative Responses; WER, WCST Incorrect Responses;
WCR, WCST Correct Responses; TMT B/A, Trail Making Test ratio B/A; STRW, Stroop Word; STRC,
Stroop Color; TMT A, Trail Making Test A; TMT B, Trail Making Test B; STRCW, Stroop Color Word; STRI,
Stroop Interference Score; WNPE, WCST Non-Perseverative Errors; , loadings under 0.001; bold numbers
indicate the highest loadings.

B/A scores loaded on the first factor (accounting for 53.06% of the variance). The
variables that loaded on the second factor (17.07% of the variance) were Stroop W,
Stroop C, Stroop WC, TMT A, and TMT B. Stroop CW and Stroop I loaded on
the third factor (9.9% of the variance). Finally, the percentage of non-perseverative
errors and TMT B/A loaded on the fourth factor (9.6% of the variance).

Statistical tests for the differences between samples

KolmogorovSmirnov tests for normality were used to determine whether the
distribution of variables fitted the normal distribution. Table 3 shows the means
and standard deviations (SD) for patients and controls, and values of significance in
the resulting t- (for normally distributed variables) and U-tests (for non-normally
distributed variables).
TBI patients showed a significantly poorer performance than healthy controls
in almost all test scores. Despite this, no differences were found in the variable
Stroop Interference (Stroop I).

Covariance analysis
Two additional analyses were performed to clarify the influence of processing speed
in the performance of TBI patients. Univaried covariance analyses were performed
in order to subtract the influence of the speed of processing from the variables
that loaded on more than one factor (Stroop CW and TMT B). This procedure
provides a very sensitive method to clarify whether the latter differences between
TBI versus control participants were the result of slower information processing
or the suggested specific attentional deficits. Thus, variables that presumably mea-
sured pure speed of processing (those which only loaded on the second factor, i.e.
Stroop W, Stroop C, and TMT A) were taken as covariates in the analysis.
 264 M. Ros et al.

Table 3. Means, standard deviations and significances for patient and control groups

Patients (n 29), Controls (n 30),

Variable mean (SD) mean (SD)  Test

STRW 81.1 (18.6) 115.8 (15.2) *** t

STRC 55.6 (14.7) 78.6 (11.6) *** t
STRCW 34.5 (10.2) 49.1 (9.1) *** t
STRI 1.8 (7.5) 2.5 (9.2) n.s. t
TMT A 59.9 (25.4) 25.5 (8.5) *** t
TMT B 162.03 (73.6) 54.4 (22.4) *** U
TMT B/A 2.9 (1.4) 2.2 (0.6) * t
WCR 65.7 (17.05) 87.07 (3.8) *** t
WER 34.3 (17.05) 12.9 (3.8) *** t
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WPE 21.7 (16.6) 6.2 (3.04) *** t

WNPE 12.4 (7.5) 6.7 (2.9) ** t
WPR 25.4 (22.05) 7.5 (2.7) *** t

***p < 0.001; **p < 0.01; *p < 0.05; n.s., non-significant differences. WPE, WCST Perseverative Errors; WPR,
WCST Perseverative Responses; WER, WCST Incorrect Responses; WCR, WCST Correct Responses; TMT B/A,
Trail Making Test ratio B/A; STRW, Stroop Word; STRC, Stroop Color; TMT A, Trail Making Test A; TMT B,
Trail Making Test B; STRCW, Stroop Color Word; STRI, Stroop Interference Score; WNPE, WCST
Non-Perseverative Errors. t, Students t-test; U, MannWhitney U-text.

Stroop CW and TMT B were selected as dependent variables for the analysis
given that both scores loaded on the processing speed factor as well as on other
different factors (third and first factor respectively). The covariance analysis had
to be performed separately because, as mentioned above, each of the dependent
variables had its own covariate, i.e. Stroop C and Stroop W were used for the
Stroop CW dependent variable, and TMT A was the covariate for the TMT B
dependent variable.
The analysis revealed that both groups did not differ significantly on Stroop CW
adjusted for both Stroop C (F(1,54) 3.510, p 0.07), and Stroop W (F(1,54)
3.691, p 0.06). Conversely, when the same covariance analysis was performed
for the TMT B adjusted for TMT A, it revealed significant differences between
groups (F(1,54) 12.802, p < 0.001).

Discussion
In this study, patients with brain injury and normal controls completed three
neuropsychological clinical tests in order to study the mechanisms underlying
attentional functioning, as well as any general differences in performance between
both groups. Recent studies have suggested that the cognitive impairment in TBI
patients measured by attentional tasks could be interpreted as an effect of a deficit in
the speed of processing instead of a specific attentional dysfunction. Factor analysis,
t- and U-tests of differences, and covariance analysis, were used to clarify the
importance of slowness in TBI patients difficulties. Although the present data
partially support the slowed processing interpretation [18, 22], the present results
also suggested that in addition to slowness, the degree of controlled processing or
supervisory strategies required to perform a task are also important factors affecting
the patient.
Significant differences were revealed by t- and U-tests between patients and
normal controls in almost all the scores. These results were in agreement with
 Attentional control and slowness of information processing after severe TBI 265

extensive evidence on the sensitivity of these three tasks in detecting TBI dysfunc-
tion [53]. First, the patients processed information significantly slower than the
healthy control group on all measures under time pressure, i.e. Stroop W, Stroop
C, Stroop CW, TMT A, and TMT B, corroborating the already well-documented
finding that slow information processing is a common consequence of TBI [39].
However, it could not be demonstrated with mean differences that the time
increases were due to attentional impairments in specific components. Covariance
analysis was performed to control the possible effect of information processing
speed on these attentional tests. A dissociation was found between the Stroop
Test and TMT results.
No disproportional distraction effect was found in the group of patients
compared with the control group when the effect of the covariates was subtracted
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from the Stroop CW condition. Patients with severe TBI did not perform worse
than controls except for the slowness of information processing. Thus, there was no
specific deficit managing conflict responses. These results have been reported in a
number of studies [1, 3, 6, 39, 54, 55]. In addition, note that the Stroop Interference
score reflected the same outcome.
Results in TMT showed that the differences between TBI patients and controls
were due to a specific attentional component impairment once the effect of the
covariate was eliminated. This result does not support the slowness only hypoth-
esis. In some TBI patients, there is a specific impairment on tasks with high
flexibility demands, resulting in mistakes when shifting from one scheme of
action to other. The TMT B/A index indicates the ability to alternate between
the two schemes and provides evidence for an attentional shift cost rather than an
explanation just in terms of the slowness of information processing.
Besides this, the experimental literature on attention shows discrepancies as to
the processes underlying performance of the tasks used and the extent to which
these tasks are redundant. Factor analytical methods clarified the type of attentional
processes involved in the studied sample. The four-factor solution obtained
accounted for 89.6% of the variance. The first factor, cognitive flexibility, incorporated
all the WCST scores included in the analysis (except non-perseverative errors),
TMT B, and TMT B/A scores. The second factor, speed of processing, included
those scores in which speed was directly measured (Stroop W, Stroop C, Stroop
CW, TMT A, and TMT B). The third factor, interference, referred to performance
decrements under distracting stimuli, and was represented by Stroop CW and
Stroop Interference scores. Two scores loaded on the fourth factor (non-persevera-
tive errors, from the WCST, and TMT B/A score) probably addressed working
memory processes.
The first factor included scores that require the ability to shift attention from
one cognitive set to another and to modify behaviour in response to changing
environmental contingencies. Perseverative responses reflect the inability to
disengage and shift attention to a new set regardless of the negative feedback
given by the examiner. TMT B and TMT B/A tap alternating attention, which
also implies the ability to shift attention from one sequence to the other. This ability
is specially identified in TMT B/A, where the influence of processing speed has
been eliminated. According to these statements, cognitive flexibility is probably the
cognitive construct underlying performance on these tests. This factor is related
to those found by other authors [5659]. However, other studies show different
results. The WCST scores do not load on a single factor by itself. It has been noted
 266 M. Ros et al.

that the literature is contradictory on this point [58]. Factor analysis data reflect
different underlying processes within WCST scores, such as cognitive flexibility and
working memory.
The second factor, named speed of processing, incorporates all measures
influenced by time pressure. No score sensitive to processing speed is left out of
this factor. Again, this finding supported evidence for a basic slowness of
information processing after moderate and severe TBI, with or without focal
frontal injuries, which is important in the subacute and chronic stage post-trauma
[18, 22]. Speed of information processing predicts future difficulties in daily
activities and has implications for employment. The relevance of this factor in
attentional models has also been established in other neurological and psychiatric
conditions, such as developmental attentional disorders, multiple sclerosis and
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schizophrenia [28, 41, 60, 61]. From a cognitive point of view, there is still a
lack of consensus as to which of the specific stages are impaired in TBI. Some
authors have postulated a slowed stimulus identification, while others have proposed
that the response selection is the principal stage that is impaired in this population
[28, 62, 63].
A third factor is described by two scores from the Stroop test. This task has been
considered a measure of cognitive interference, especially in the incongruent con-
dition (Stroop CW). The finding that Stroop CW and Stroop Interference load on
the same factor suggested the presence of a cognitive process that requires control
over the automatic and prepotent response tendency. The two scores taping this
mechanism load on the third factor regardless of the time pressure influence. This
factor, showing the ability to control distractibility to irrelevant stimuli, is one of
the most consistent findings in the attentional literature [56, 64].
The common process shared by the two scores loading on the fourth factor
is probably working memory. The most complex component of TMT requires the
ability not only to shift attention from one sequence to the other, but also to
maintain both sets active, so they are ready to be recalled. The influence of working
memory on the WCST performance is also well documented [6567]. Recent
research [68, 69] has suggested that the ability to switch attention strongly depends
on working memory processes, particularly on the phonological loop. There
are also neurophysiological findings supporting the view that working memory
and set-shifting cooperate in the same areas of prefrontal cortex and therefore
enable us to adapt to changing environments [70, 71]. This remains, however, an
area for further exploration.
As mentioned above, other authors have clustered the factor solution in two
different dimensions: speed and control, related to low- and high-level processes.
While the second factor appeared to be particularly sensitive to scores highly influ-
enced by time pressure, the scores loading on the first, third and fourth factors
reflected aspects of attentional control. Nevertheless, the present data suggested
that the control process of attention might be better considered in terms of separate
capacities or processes: interference control, cognitive flexibility and working
memory (figure 1). The complexity of attentional processes has been emphasized
elsewhere [72]. The large domain of attentional control appears to be highly
heterogeneous and there is much left to explore in this area.
Several limitations of the present study should be noted. In respect to the factor
analysis, it would be interesting to include specific measures for processes such as
working memory and other attentional control components (PASAT, digit symbol,
 Attentional control and slowness of information processing after severe TBI 267
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Figure 1. Results obtained from the factor analysis performed on three classical measures of executive attention
(WCST, TMT, Stroop tests). The four-factor solution was clustered in terms of two different dimensions:
speed of information processing and control, related to low- and high-level processes, respectively. In line with
recent electrophysiological and neuro-imaging evidence [70, 78, 79], the present results support the view
that control processes should be considered in terms of relatively independent but interrelated subprocesses
(i.e. cognitive flexibility, interference control and working memory).

BTA, etc.) for a better definition of the mechanisms that underlie and control the
attentional processes. This would help in the understanding of the influence of
information processing speed on complex attentional mechanisms. Factor four
should be examined in future research to identify clearly what kind of processes
underlie its functioning and to detect the role of this process in the performance of
these tests. Working memory could be considered to mediate high-level processes,
according to the idea that attention components (maintenance of attention, selec-
tion of target information, capacity of information-processing ability, alternating
attention between tasks) rely on working memory and the central executive
processes [40, 73].
The sample of this investigation presents a very high educational level. This fact
probably has some influence on the results obtained limiting their generalization
to groups of patients outside this range. To reduce this influence, a whole range
of educational levels should be included or, alternatively, the weight of this
characteristic on different attentional measures should be studied.
The high variability found in the patient group could point to different
subgroups of patients whose performance is mediated by the speed of information
processing rather than by the acuity of response, and vice versa. This fact contributes
to explain the lack of agreement among researchers about the presence of different
patterns of attentional impairment. Future research should address variables such
as time lapse since injury, neuropathological changes, etc.
 268 M. Ros et al.

Despite these methodological weaknesses, the present study has added to

previous research providing highly influential evidence on clinical and theoretical
grounds.
With respect to neuropsychological assessment, it is well known that test results
might be interpreted in many ways because a test never taps only one but a
whole range of cognitive functions, requiring several different skills for completion
[38, 74]. The present study has contributed to the understanding of which scores
from each test are related to different attentional mechanisms underlying per-
formance (i.e. interference and TMT B/A were shown to be the best indexes for
tapping the control process in Stroop test and TMT, respectively).
There is a trade-off between speed and accuracy in TBI patients execution
where quality of performance could improve by slowing down the pace at which
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information is presented. Time pressure could lead to misinterpretation of the results

of most neuropsychological tests administered to TBI patients, overlapping the
effects of low- and high-level deficits. Further research is needed to extend and
apply our knowledge to design tasks that explore attentional and central executive
functions free from time pressure. This would allow the differentiation of these
variables, as it is impossible to assume that the routine information processes are
intact in TBI patients [18, 39].
Taking into account the factors proposed and the clustering of the tests used,
a relatively broad battery of tests is necessary to assess the different components
of the attentional network. Some training approaches have been developed from
various models to treat different aspects of attention (sustained, selective, divided,
etc.) [35, 75, 76]. If slow processing is a basic problem underlying attentional
impairments after TBI and has a wide range of effects in the life of head injury
patients, it should be a prime target for cognitive rehabilitation. In recent years, if
the executive component of attentional processes is preserved [77], programmes
have included plans to teach compensatory and learning strategies in order that
patients can manage time pressure in everyday activities such as preparing a meal,
holding a conversation, or driving a car. Patients who only suffer from slow infor-
mation processing may be able to compensate for these deficits or adapt to the new
situation by restructuring activities. However, it is important to assure that the
attentional control components are intact for this group of patients, and hence
further research and exploration are necessary.

Acknowledgements
Work was partially supported by the Obra Social de Caja de Madrid. The authors
thank Dr Richard Thomas (Institute of Cognitive Neuroscience, UCL, London),
Dr Gabriela Grizb (UNED), and Dr Francisco Barcelo (UIB), for providing
comments on earlier versions of this manuscript.

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