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Neurocognitive Enhancement Therapy With Work Therapy
Effects on Neuropsychological Test Performance
Morris Bell, PhD;
Gary Bryson, PhD;
Tamasine Greig, PhD;
Cheryl Corcoran, MD;
Bruce E. Wexler, MD
Arch Gen Psychiatry. 2001;58:763-768.
ABSTRACT
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Background Cognitive deficits are a major determinant of social and occupational
dysfunction in schizophrenia. In this study, we determined whether neurocognitive
enhancement therapy (NET) in combination with work therapy (WT) would improve
performance on neuropsychological tests related to but different from the
training tasks.
Methods Sixty-five patients with schizophrenia or schizoaffective disorder were
randomly assigned to NET plus WT or WT alone. Neurocognitive enhancement therapy
included computer-based training on attention, memory, and executive function
tasks; an information processing group; and feedback on cognitive performance
in the workplace. Work therapy included paid work activity in job placements
at the medical center (eg, mail room, grounds, library) with accompanying
supports. Neuropsychological testing was performed at intake and 5 months
later.
Results Prior to enrollment, both groups did poorly on neuropsychological testing.
Patients receiving NET + WT showed greater improvements on pretest-posttest
variables of executive function, working memory, and affect recognition. As
many as 60% in the NET + WT group improved on some measures and were 4 to
5 times more likely to show large effect-size improvements. The number of
patients with normal working memory performance increased significantly with
NET + WT, from 45% to 77%, compared with a decrease from 56% to 45% for those
receiving WT.
Conclusions Computer training for cognitive dysfunction in patients with schizophrenia
can have benefits that generalize to independent outcome measures. Efficacy
may result from a synergy between NET, which encourages mental activity, and
WT, which allows a natural context for mental activity to be exercised, generalized,
and reinforced.
INTRODUCTION
COGNITIVE DEFICITS in schizophrenia limit social and vocational functioning1, 2, 3, 4, 5
and persist after treatment with currently available pharmacotherapies. It
is therefore important to evaluate new treatment approaches for these debilitating
aspects of the illness.
In the present project, we sought to induce activity-dependent enhancement
of underfunctioning (and underused) neurocognitive systems in patients with
schizophrenia. We had patients begin by practicing attention and memory tasks
made easy enough for them to perform successfully. Tasks were made incrementally
more difficult as successive levels were mastered. Previously, we found that
following this approach, patients were able to attain normal and even supranormal
levels of performance on tasks on which they initially showed performance
deficits.6 Moreover, we found a correlation
between the degree of functional improvement and the degree of normalization
of frontal lobe activation during task performance as measured by functional
magnetic resonance imaging.7 We are not aware
of research studies of other similarly intensive and extended repetitive training
programs, but there are several reports of positive effects of more limited
training on response speed,8 sustained attention,9, 10, 11 and problem solving.12, 13 Moreover, elemental cognitive training
has been incorporated into comprehensive rehabilitation programs with promising
preliminary results.14, 15, 16
In the present study, we evaluated the effects of repetitive practice
of progressively more difficult computerized attention and memory tasks in
the context of a work therapy (WT) program. Patients were randomly assigned
to receive WT alone or neurocognitive enhancement therapy plus WT (NET + WT).
In addition to the training of elemental cognitive functions, NET included
biweekly feedback on cognitive performance in the workplace and a weekly social
information processing group. These treatment elements provided ongoing opportunities
to incorporate elemental neurocognitive gains into more complex cognitive
operations. In addition, since WT alone is clinically efficacious,17, 18, 19 it provided an active
control condition against which to compare the effects of NET.
To our knowledge, this study is the first to combine methods of cognitive
training with WT. Its elements interact to maximize the likelihood that cognitive
training will generalize to vocational outcomes. This report focuses exclusively
on cognitive outcome data, after 5 months of treatment, for the first 65 patients
enrolled. When the study is completed, subsequent reports will describe intergroup
comparisons of work performance and vocational outcomes.
SUBJECTS AND METHODS
SUBJECTS
Sixty-five patients with schizophrenia or schizoaffective disorder,
as determined by PhD-level psychologists using the Structured Clinical Interview
for DSM-IV procedures,20
participated after being referred by their clinicians. All provided informed
written consent. Patients were receiving treatment at the Veterans Affairs
Medical Center, West Haven, or at the Connecticut Mental Health Center, New
Haven. Patients were not considered sufficiently stable to participate if
there had been a change in psychiatric medications or housing in the last
30 days, if they had an episode of drug abuse within the past 30 days, or
if they had a Global Assessment of Functioning score of 30 or less. Known
neurological disease and developmental disability also were causes for exclusion.
All patients were receiving antipsychotic medication prior to and throughout
the study. Fourteen (22%) were receiving a typical antipsychotic drug only,
45 (69%) were receiving an atypical antipsychotic drug only, and 5 (8%) were
receiving both, with comparable proportions and dosages for NET + WT and WT
conditions.
BASELINE AND OUTCOME ASSESSMENTS
Neuropsychological testing for pretest-posttest comparisons consisted
of (1) Digit Span, Letter Number Sequencing, and Digit Symbol Substitution
Task from the Wechsler Adult Intelligence Scale–III21
(WAIS-III); (2) Visual Reproduction I and II, Figural Memory, and Logical
Memory I and II from the Wechsler Memory Scale–Revised (WMS-R)22; (3) the Hopkins Verbal Learning Test (HVLT), a measure
of verbal learning and temporal lobe dysfunction23;
(4) the Continuous Performance Test,24 a measure
of sustained attention; (5) Wisconsin Card Sorting Test (WCST),25, 26
a measure of perseveration and flexibility of abstract thought; (6) Bell Lysaker
Emotion Recognition Task (BLERT),27 a measure
of the ability to identify affect cues in videotaped stimuli; (7) Gorham's
Proverbs Test,28, 29 a measure
of thought disorder; (7) Hinting Task,30 a
measure of social inference; and (8) Trail-Making Test–B,31
a measure of cognitive flexibility and psychomotor speed. These measures have
established reliability and validity and are sensitive to the types of deficits
associated with schizophrenia.
Work performance was assessed using the Work Behavior Inventory.32, 33 The Work Behavior Inventory provides
6 measures of work performance, which include 5 scales (social skills, cooperativeness,
work habits, work quality, and personal presentation) and a general score
of overall performance. Our studies have found excellent internal consistency,
factorial validity, concurrent validity with the Work Personality Profile,34 and interrater reliabilities of 0.89 to 0.93 for
scale scores. Cognitive assessment in the workplace was performed using the
Cognitive Functional Assessment scale,35 which
has 3 subscales: attention/concentration, memory/learning, and executive functions.
Interrater reliability intraclass coefficients for our group are in the good
to excellent range (r = 0.75 to 0.91).
Symptoms were rated using the Positive and Negative Syndrome Scale,
which was scored according to a 5-component model.36
Interrater reliability intraclass coefficients were in the excellent range
for component scores (r = 0.88 to 0.93).37
PROCEDURES
Following informed consent, neuropsychological testing was performed
over 2 or 3 sessions and again 5 months after the beginning of the active
intervention. Psychologists (PhD or master's level) who were trained specifically
in study methods performed all procedures. Following intake testing, patients
were stratified based on degree of cognitive impairment and randomly assigned
to NET + WT or WT conditions. Significant cognitive impairment was based on
6 key neuropsychological indicators in 4 cognitive domains: (1) attention
was represented by the Continuous Performance Test total score wrong; (2)
memory was represented by HVLT Trial 1 and WMS-R Figural Memory; (3) executive
function was represented by WCST categories correct and Gorham's Proverbs
Bizarreness; and (4) affect recognition was represented by BLERT total score
correct. A patient must score 1 SD below the mean (established for a Veterans
Affairs Medical Center sample of patients with schizophrenia) on at least
2 indicators to be so classified. Twenty-eight patients (43%) met these criteria.
Work therapy consisted of (1) payment for work activity at the rate
of $3.40 per hour for up to 15 hours per week with increasing bonus pay ($3.90
to $8.40) for 16 to 20 hours; (2) job placement at this medical center; (3)
individual counseling when problems arise; (4) a group offering support, problem
solving, detailed work performance feedback based on the Work Behavior Inventory,
and goal setting; (5) a job coach for job-related difficulties and individual
vocational counseling; (6) a certificate of participation in the program;
and (7) referral to other vocational services. The most common work sites
were in the dietetics department, mail room, grounds, maintenance department,
patient transport, and medical administration, with duties similar to those
of entry-level employees supervised by regular medical center personnel.
Neurocognitive enhancement therapy consisted of (1) feedback from the
Cognitive Functional Assessment in the support group, (2) cognitive exercises
for up to 5 hours each week for 26 weeks, and (3) a weekly social processing
group. Patients were paid for doing cognitive exercises at $3.40 per hour
with increasing bonus pay for reaching a maximum of 5 hours of cognitive training.
They could also work up to 15 hours in WT for a combined maximum of 20 hours
of productive activity per week.
Cognitive Functional Assessment feedback was given on a biweekly schedule
(at the same time patients receive the Work Behavior Inventory feedback) and
consisted of ratings of attention, memory, and executive function from their
job. Patients were also encouraged to develop goals based on their Work Behavior
Inventory and Cognitive Functional Assessment feedback.
Cognitive exercises involved repeated practice on computer-based exercises
for attention, memory, and executive function (adapted to our specification
by Odie Bracy, PhD, Neuroscience Center, Indianapolis, Ind) and a dichotic
listening task. Patients attended 2 to 3 sessions per week. Cognitive exercises
used a modified form of Psychological Software Services CogReHab software,38 a multimedia cognitive rehabilitation software designed
for use with individuals with compromised brain function. Four tasks were
modified from this software package: 2 tasks (Visual Tracking I and Visual
Tracking II) for training sustained visual attention and 2 tasks (Sequence
Recall: Digits-Visual and Sequence Recall: Words-Visual) for training verbal
memory. A fifth task (Pyramids) was used to train executive functions. Task
parameters were initially made easy enough for each patient to do well. As
soon as the patient was able to achieve 90% accuracy at a given difficulty
level, the task was made more difficult following a prearranged hierarchy.
Details of the tasks are described below.
Visual Tracking I begins with a black line moving across the computer
screen against a red background. As this line moves, yellow cubes appear along
the line. The patient is required to focus visually at the end of the line
and click the left mouse button whenever a yellow cube appears. The patient
hears a "TA DA" sound if correct and a wrong chord sound if the patient responds
when no yellow cube is present. Data on the percentage of hits and misses
are collected. Changing the speed of the black line's movement or the duration
of the task increases task difficulty.
Visual Tracking II begins with a red circular shape moving about the
computer screen in a random pattern against a black background. The patient
is required to visually focus at the center of the circle and must press the
mouse button when the circle turns yellow. Changing how fast the circle moves
around the screen or duration of the task modifies difficulty. Feedback and
scoring are the same as for Visual Tracking I.
Sequence Recall: Words-Visual begins with displaying a list of 2 to
10 words on the computer screen for the patient to remember in order. After
a delay, one of the words is presented again and the patient must click on
a numbered line to indicate its position from the original list. Correct responses
produce the "TA DA" sound and incorrect responses produce a wrong chord sound.
The number of correct and incorrect trials is totaled. Task difficulty is
modified by changing the length of the list, the number of times a list is
presented, the amount of time to study the list, and the length of the delay
between the presentation of the list and the presentation of the target word.
Sequence Recall: Digits-Visual begins with a list of 2 to 10 digits
displayed one at a time on the computer screen. The patient must remember
the digits in order. After a delay, the patient follows the same procedure
described for words. Data collection and procedures for modifying task difficulty
are also the same as for the words task.
In the Pyramids task, the computer screen displays 3 playing posts with
the left post containing 3 to 5 disks stacked in a pyramid. The patient is
required to have the disks form a pyramid on the right post by moving the
disks, one at a time, from the left post. The program will not allow placement
of a larger disk on a smaller one. Data on the number of moves, task duration,
and whether the task was solved are collected. Changing the number of disks
to move modifies task difficulty.
The dichotic listening task requires the patient to listen to a story
in the right ear of a headphone set while ignoring poetry heard in the left
ear. After listening to a story segment for 30 to 90 seconds, the story and
poem are paused and a question regarding the just completed segment is asked.
The patient listens to 8 story segments and is scored on the number of correct
answers. The distracter (poem) is initially presented at a very low volume
and the volume is gradually increased as the patient progresses to harder
levels. Eventually the distracter volume is greater than the story volume.
The volume of the story remains constant, but the length of the story segments
is increased for greater task difficulty.
The weekly group for social information processing is similar to a group
exercise from the traumatic brain injury program of Ben-Yishay et al.39 One subject each week prepares an oral presentation,
with staff assistance, that is delivered to the group. Each group member is
required to ask a question and give specific feedback to the presenter. Three
topics are given sequentially over the 6 months: "My job," "A day at work,"
and "What I've learned." This highly structured group experience demands verbal
expression, verbal memory, and executive function, as well as social information
processing, affect recognition, and interpersonal sensitivity.
DATA ANALYSES
An intent-to-treat analysis was employed, which used all patients randomized
to a condition regardless of degree of participation. From the neuropsychological
testing battery, 21 variables were identified that represented the most important
cognitive demands of each test. To reduce experiment-wise error, a factor
analysis of intake data was used to determine which variables could be grouped
by shared variance. These groupings could then be used as dependent measures
in multivariate analysis of covariance (MANCOVA). A principal components analysis
followed by varimax rotation of intake data revealed that 20 of the 21 variables
could be included in a 4-factor solution with eigenvalues greater than 1.5.
Failure to maintain set from the WCST was the only variable not included in
the 4-factor solution. MANCOVAs were performed on follow-up scores with intake
scores as the covariate on each set of variables from the 4-factor solution.
Effect-size comparisons were made using  2 statistics on variables
that showed significant differences between groups. Parametric procedures
were 2-tailed, and  was set at .05 for all analyses.
Finally, a comparison between groups was performed on the number of
patients whose scores went from abnormal to normal by using McNemar's Qm, a nonparametric between-groups analysis. McNemar Qm is
a conservative test of change because it does not capitalize on the fact that
WT showed a slight decline in the percentage of patients whose test scores
at follow-up were within the normal range. We defined normal performance using
published norms for each instrument. For WCST percent conceptual level responses
and percent nonperseverative error, which are standardized scores based on
published norms,25 we defined normal as a standardized
score of 90 or greater. For the BLERT, we defined normal as a score of 15
(of 21) or better. In a normative sample of 81 college students, all performed
within that range compared with 72% of substance abusers and 42% of patients
with schizophrenia or schizoaffective disorder.27
We defined normal functioning on the Digit Span Backward task as performing
within 2 digits of the subject's Digit Span Forward task performance. This
criterion is based on normative tables21 that
indicate that most normal subjects will recall digits backward within that
range. By basing "normal" on each person's Digit Span Forward performance,
we were also taking into account the effect of increased Digit Span Forward
performance that might have resulted from the cognitive training. Thus, if
a patient could recall 6 digits forward at intake, he/she would need to recall
4 digits or more at intake to be within normal limits. If the patient improved
to 7 digits forward at follow-up, he/she would then need to recall 5 digits
or more backward to be categorized as having a performance within the normal
range.
RESULTS
GROUP COMPARISONS: MANCOVAs
No significant differences were found between NET + WT and WT groups
at baseline for illness, treatment, or background characteristics (Table 1). However, MANCOVAs of pretest-posttest
neuropsychological variables as they were grouped by factor analysis showed
significant differences between conditions.
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Table 1. Background and Treatment Characteristics*
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Factor 1 (WCST factor) consisted entirely of WCST variables and MANCOVA
indicated a significant difference between groups (F4,55 = 3.97; P<.006). Least square means, which adjust follow-up
means by the intake scores, are shown in Table 2. Standardized scores for WCST variables were used so that
a higher score represents better performance. Categories correct is not standardized.
All findings favored NET + WT. Factor 2 (working memory factor) included BLERT
total score, WAIS-III Digit Span Forward, WAIS-III Digit Span Backward, WAIS-III
Letter Number Sequencing, WAIS-III Digit Symbol, WAIS-III Digit Symbol Substitution
Task, and Trail-Making Test–B total time. With the exception of Digit
Span Forward, these variables have in common advanced processing and manipulation
of information. This involves accurately absorbing information and retaining
it in working memory while taking mental action on it. MANCOVA revealed significant
group differences on these variables (F6,47 = 3.07; P<.01), with all findings favoring NET + WT.
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Table 2. Least Square Mean Differences From Multivariate Analyses of
Covariance for Pre-Post Neuropsychological Testing*
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Factor 3 (thought disorder factor) consisted of WMS-R Logical Memory
I, WMS-R Logical Memory II (30-minute delay), Hinting Task, and Gorham's Proverbs
Bizarreness score. These variables have in common disorganization of thought
and language. MANCOVA did not reach significance (F4,50 = 0.94, P = .45). Factor 4 (visual and verbal recall) consisted
of HVLT Trial 1 total score, HVLT Trial 3 total score, WMS-R Visual Recall,
WMS-R Visual Recall with 30-minute delay, Continuous Performance Test correct,
and WMS-R Figural Memory. This factor consisted of visual and verbal memory
tasks that did not require manipulation of information in working memory.
MANCOVA showed no group differences (F6,50 = 1.14, P = .35).
AFFECT RECOGNITION AND WORKING MEMORY
Having found significant group differences on working memory and affect
recognition variables, we compared the conditions on their frequency of patients
with large (>0.8 SD), small (>0.2 SD), or no effect-size changes. On the BLERT,
20 NET + WT patients (65%) had small or large effect-size improvements compared
with 10 (29%) of WT patients (21 = 8.04, P = .005) and 12 (39%) had large effect-size changes compared
with 3 (9%) of WT patients (22 = 10.18, P = .006). For Digit Span Backward, 21 (68%) of NET + WT patients had
small or large effect-size improvements compared with 12 (35%) of WT patients
(21 = 6.83, P = .009)
and 12 (39%) had large effect-size changes compared with 6 (18%) of WT patients
(22 = 6.98, P = .03).
Although these findings indicate that more NET + WT patients improved
their affect recognition and working memory, the most stringent test for the
clinical significance of an intervention is whether it can return patients
to normal levels of function.40 The percentage
of NET + WT patients with normal scores on the BLERT increased from 35% to
60%, whereas the percentage of WT patients with normal scores declined from
47% to 42% (Qm1 = 4.03, P<.05). The
proportion of NET + WT patients with normal Digit Span Backward performance
increased from 45% at intake to 77% at follow-up, whereas the proportion of
WT patients with normal performance on this task decreased from 56% to 45%
(Qm1 = 6.41, P<.01).
IMPROVED EXECUTIVE FUNCTION
For percent conceptual level, 18 (58%) of NET + WT patients had small
or large effect-size improvements compared with 11 (32%) of WT patients (21 = 4.4, P = .04) and 11 (35%)
had large effect-size changes compared with 4 (12%) of WT patients (22 = 5.92, P = .05). For nonperseverative
error, 16 (52%) of NET + WT patients had small or large effect-size improvements
compared with 6 (18%) of WT patients (21 = 8.36, P = .004) and 5 (16%) had large effect-size changes compared
with 1 (3%) WT patients (22 = 8.727, P = .01).
The proportion of patients with percent conceptual level responses within
the normal range increased from 39% to 48% for NET + WT and from 29% to 42%
for WT. The proportion of patients with nonperseverative error within the
normal range increased from 45% to 52% for NET + WT patients and decreased
slightly, from 47% to 42%, for WT patients. Between-group differences in proportional
change were not significant for these 2 tasks.
COMMENT
These results support the efficacy of NET + WT and show that cognitive
retraining increased neuropsychological functioning to a degree not achievable
from the nonspecific cognitive stimulation that comes from work activity alone.
These analyses indicate that patients receiving NET + WT showed greater mean
differences and more large effect-size changes than did patients receiving
WT alone. Moreover, NET + WT demonstrated clinical significance. The number
of patients in the NET + WT group with performances within normal limits increased
to 60% for a test of affect recognition and increased to 77% on a test of
working memory (Digit Span Backward in relation to Digit Span Forward).
Compared with WT, NET + WT led to greater improvement in executive functioning
as measured by WCST variables. The same was true for tasks that required holding
information in working memory and taking action on it. However, the factor
consisting of tasks sensitive to conceptual and language disorganization and
the factor with verbal and nonverbal secondary memory tasks did not show differential
improvement for NET + WT. It is somewhat surprising that cognitive exercises
that so heavily relied on computer-based practice of elemental cognitive functioning
such as attention and short-term memory should have had greater effect on
executive function, manipulation of information in working memory, and affect
recognition than on simpler memory tasks. It may be that the social information
processing group, dichotic listening, and cognitive feedback from the work
site, which were also part of NET and which demand executive function and
affect recognition, affected this outcome. It is likely that it is the interaction
of all these elements of NET in combination with WT that is responsible for
these favorable neuropsychological outcomes. The fact that more than one third
of the group receiving NET + WT showed large (>0.8 SD) effect-size improvements
on some tests and that a significantly greater proportion of patients achieved
normalization of cognitive function on some tasks indicates that treatments
such as NET + WT may have clinical as well as statistical significance. There
may be a true synergy between NET exercises that encourage mental activity
and WT that allows a natural context for increased mental activity to be exercised,
generalized, and reinforced.
Our next step in this investigation will be to compare groups on clinical,
quality of life, and vocational outcomes at 6 months after intake. If we find
that NET leads to greater improvement in these outcome domains, we will attempt
to associate improvements in neuropsychological pretesting and posttesting
as a mediating variable. In so doing we will learn the extent to which improvements
in test performance predict functional outcomes.
This study did not control for the amount of productive activity patients
could engage in except to have a maximum of 20 paid hours of work per week.
However, patients in both conditions were productive for about the same number
of hours and received about the same amount of pay over the 6-month course
of the intervention. Although NET + WT patients may have had somewhat more
time for nonspecific interactions with research staff around the NET procedures
(which were mostly computer based), WT patients had more time for interactions
with coworkers and supervisors, which may have been equivalent in terms of
their likely effects on cognitive functioning. This study is also limited
by not having a no-treatment control that would have helped us to sort out
the likely contribution of WT to cognitive outcomes. We also did not perform
imaging studies to determine how NET + WT may have affected brain function
or structure, and we do not know how enduring the cognitive improvements might
be. In future studies, we hope to redress these weaknesses.
AUTHOR INFORMATION
Accepted for publication February 26, 2001.
This work was funded by a grant from the Rehabilitation Research and
Development Service, Department of Veterans Affairs (Dr Bell), and a Career
Development Award from the National Institute of Mental Health, Rockville,
Md (Dr Wexler).
From the Veterans Affairs Connecticut Healthcare System, West Haven,
Conn; and Department of Psychiatry, Yale University School of Medicine, New
Haven, Conn.
Corresponding author and reprints: Morris Bell, PhD, Psychology Service
116B, 950 Campbell Ave, VA Connecticut Healthcare System, West Haven, CT (e-mail: Bell.Morris_D+{at}West-Haven.va.gov).
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