You are on page 1of 18

DOI: 10.

1093/brain/awg237 Advanced Access publication July 22, 2003 Brain (2003), 126, 2363±2380

Staying on the job: the frontal lobes control


individual performance variability
Donald T. Stuss,1 Kelly J. Murphy,1,3 Malcolm A. Binns1 and Michael P. Alexander2
1Rotman Research Institute, Baycrest Centre for Geriatric Correspondence to: D. T. Stuss, Ph.D., The Rotman
Care and University of Toronto, Toronto, Ontario, Research Institute of Baycrest Centre, 3560 Bathurst

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


Canada, and 2Harvard Medical School, Boston, MA, USA Street, Toronto, ON, M6A 2E1 Canada
E-mail: dstuss@rotman-baycrest.on.ca
3Present address: Psychology Department of Baycrest
Centre for Geriatric Care, Toronto, Ontario, Canada

Summary
The causes of variability of performance by individual patients and 10 controls returned for two subsequent
subjects have rarely been investigated, although exces- test sessions, which permitted the assessment of consist-
sive variability or inconsistency may be a functionally ency of performance. Measures of abnormal dispersion
signi®cant factor for many real-life activities. Our of performance on these tests were observed in frontal
objective was to determine whether patients with focal patients only (except those with exclusively inferior
frontal brain lesions have excessive individual perform- medial damage). Disturbances in consistency of per-
ance variability. Thirty-six patients with focal frontal formance were observed primarily in patients with
(n = 25) or non-frontal (n = 11) lesions were compared frontal lesions. Damage to the frontal lobes impairs the
with 12 control subjects on different measures of intra- stability of cognitive performance. Damage to different
individual variability: dispersion within a testing ses- frontal regions causes different pro®les of abnormal
sion; and consistency across testing sessions. Four reac- variability. Fluctuations in performance of a task may
tion time tasks, varying in levels of complexity and underlie some of the reported dif®culties in daily tasks
based on a model of detection using feature integration, reported by patients with frontal injuries.
were administered. Following the ®rst test session, 22

Keywords: frontal lobes; reaction time; individual differences; intra-individual variability; attention

Abbreviations: CTL = control; DL = dorsolateral; ICV = intra-individual coef®cient of variation; IIV = intra-individual
variability; IM = inferior medial; ISD = intra-individual standard deviation; LDL = left dorsolateral; NF = non-frontal;
RDL = right dorsolateral; RT = reaction time; SM = superior medial; TBI = traumatic brain injury; TSI = time since
injury.

Introduction
Analysis of quantitative neuropsychological tests requires Variation of performance of an individual subject may also
consideration of performance variability on the tests. There contribute `noise'. It may also be a source of considerable
are different types of variability and they have different information (Flugel, 1928; Philpott, 1933; Fiske and Rice,
consequences for analysis of different methods of control. 1955; Cronbach, 1957; Barratt, 1963) and there is a substan-
Diversity is the variation of performance between subjects in tial history of studying intra-individual variability (IIV) as the
a group; it is inter-individual variability and is usually viewed dependent measure of interest (Stuss et al., 1989). IIV is
as `noise'. Diversity is sometimes successfully controlled by short-term ¯uctuation in performance, not the durable and
methodological techniques: using a consistent test environ- systematic change due to practice, learning, developmental
ment; creating homogeneous groups; the extreme example growth, trait alterations or, in clinical practice, improvement
being single subject studies; or using very large groups or progression of the medical problem. There are two general
(Cronbach, 1957). types of IIV. Dispersion is the oscillation of performance by
Brain 126 ã Guarantors of Brain 2003; all rights reserved
2364 D. T. Stuss et al.

an individual during a single continuous task. Consistency is cognitive domain, and this form of increased IIV has been
the degree of variability of an individual between adminis- most consistently described in patients with `executive'
trations on the same test either within the same testing impairments, with or without overt demonstration of focal
session, or over separate sessions of testing. The foci of the frontal lesions.
present study are dispersion and consistency.

Trauma
Factors affecting variability of performance Since the initial report of Goldstein (Goldstein, 1942)
It is dif®cult to generate detailed predictions about the causes demonstrating increased IIV (and overall slow RT), numer-
of IIV from prior studies because of differences in working ous studies have con®rmed increased dispersion or reduced

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


de®nitions of variability, task demands, statistical methods consistency in patients with traumatic brain injury (TBI) at all
and subject populationsÐsome normal and others clinical. levels of severity, with or without focal frontal lesions (Stuss
There are, however, some factors that have been identi®ed as et al., 1989, 1994b; Whyte et al., 1995; Collins and Long,
possible contributors to IIV. Increased age is frequently cited 1996; Hetherington et al., 1996; Spikman et al., 1996;
as a cause of greater variability of performance and of Segalowitz et al., 1997; Bleiberg et al., 1997, 1998; Zahn and
inconsistency (Fozard et al., 1994; Shammi et al., 1998; Mirsky, 1999).
Anstey, 1999), but this aging effect is task or measurement
dependent (Foster et al., 1995; Lindenberger and Baltes,
1997; Shammi et al., 1998). Normal aging (Salthouse, 1993, Dementia
1996; Fozard et al., 1994) and many neurological disorders Patients with a variety of dementing illnesses are also
(van Zomeren and Brouwer, 1994; Whyte et al., 1995; Collins reported to be more variable in performance than normal
and Long, 1996; Bleiberg et al., 1998; Leth-Steensen et al., elderly (Hultsch et al., 2000). There is an apparent ordering of
2000) produce a general slowing on numerous reaction time the level of variability in different dementing disorders.
(RT) tasks, and overall RT slowing may be accompanied by Patients with Lewy body disease exhibit the greatest ¯uctu-
variability of RT. The association is not suf®cient to account ation of performance, followed by vascular dementia and then
for all variability in RT performance. In some experiments, Alzheimer's disease (Walker et al., 2000; Ballard et al.,
no association has been found between overall RT and IIV 2001). Murtha et al. (2002) showed that patients with frontal±
(Benton and Blackburn, 1957; Bruhn and Parsons, 1971; temporal dementia have more IIV than those with
Schwartz et al., 1989; Hetherington et al., 1996). In other Alzheimer's disease.
reports, the correlation between overall RT and IIV has been
quite inconsistent depending on the exact variability measure
(Shammi et al., 1998). Miscellaneous
Tasks that appear to require more active control of Increased IIV has also been reported in schizophrenia (but not
attention are often labelled `complex', although complexity affective disorders) (Schwartz et al., 1989), and in attention
can surely be generated along many task dimensions. Perhaps de®cit disorder and conduct disorder (Zahn et al., 1991; Leth-
because of differences in working de®nition, complexity has Steensen et al., 2000).
had a mixed effect on performance variability. In some In both normal subjects and clinical groups, IIV is sensitive
studies, task complexity increased IIV (Stuss et al., 1994b; to `executive control'. In normal subjects, IIV is sensitive to
Shammi et al., 1998; West et al., 2002b) but, in others, it did the demand for executive control (Shammi et al., 1998; West,
not (Bruhn and Parsons, 1971; Zahn et al., 1991; Foster et al., 1999a). In normals, West et al., (2002b) concluded that
1995). increased IIV was limited `almost exclusively' to task
Whether the mechanism of increased IIV is due to some conditions requiring the active demands of such executive
aspect of complexity or to slower overall responses or to some control processes. In TBI, IIV is closely associated with
other fundamental psychophysiological process, it has been impaired maintenance of consistent `top-down' attentional
observed for many years that brain damage causes increased processes (Stuss et al., 1989, 1994b; Stuss, 1991). The
IIV (Head, 1926; Goldstein, 1942; Benton and Blackburn, hierarchy of IIV in dementias parallels the relative frontal
1957). This variability may be of two general types. There system damage; individuals with Alzheimer's disease have
may be increased IIV that is speci®c to a discrete cognitive the least involvement of the frontal lobes and the least IIV.
process, and probably always associated with impairment to There have been no direct experiments to determine
that process. Thus, patients with right brain damage and whether lesions in any focal region of the frontal lobes are
spatial neglect show increased variability on bisection tasks critical in the production of increased IIV, but there is indirect
(Anderson et al., 2000) and patients with left brain damage evidence that suggests that right dorsolateral (RDL) lesions
and aphasia appear to show increased IIV on lexical decision may be particularly likely to increase IIV. Right frontal
tasks (Milberg et al., 2003). There may also be increased IIV lesions impair top-down attentional control (Fink et al.,
due to a general de®cit in regulation of attention to any task. 1997). Patients with right frontal lesions make excessive
The general de®cit would not be associated with any distinct errors due to a lowered inhibition to distracting information
Individual variability in reaction time 2365

Table 1 Aetiology, lesion location, lesion size*, time since injury and handedness within patient groups
Subject Aetiology Lesion location Lesion size (%) TSI (months) Handedness

LDL frontal
1019 Trauma DL, ACG, IM, polar 0.87 31.1 Right
1021 Stroke DL 1.03 2.8 Right
1027 Stroke DL, polar, medial 3.76 18.3 Right
1029 Stroke DL 1.76 24.0 Left
1053 Trauma DL 0.92 291.1 Right
2012 Tumour DL, SM, ACG 1.46 3.8 Right

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


RDL frontal
1017 Stroke DL, parietal 3.04 1.3 Left
1041 Lobectomy DL, IM 2.92 4.2 Right
1054 Tumour IM, DL, ACG 2.55 24.7 Right
1055 Stroke SM, DL 5.09 10.9 Right
1067 Stroke DL 0.84 21.0 Right
2001 Stroke DL, striatal 3.26 5.3 Right
2024 Stroke DL, striatal 1.74 2.5 Right

IM
1023 Stroke Striatal, caudate, IM(L), ACG(L) 0.85 26.7 Both
1056 Stroke IM, ACG 1.60 33.1 Both
1059 Trauma IM, DL, ACG 4.47 34.1 Left
1065 Trauma IM 1.30 15.6 Right
1069 Tumour IM 0.22 2.5 Right
2013 Stroke IM, septal, ACG 0.07 8.9 Right

SM (+ IM)**
1011 Trauma Medial, DL(L), ACG 7.17 13.9 Right
1044 Stroke IM, polar, ACG, SM(L) 3.20 118.9 Right
2002 Stroke Medial, DL, ACG(L) 1.19 4.6 Right
2011 Stroke SM, ACG 1.60 3.6 Right
2045 Stroke Medial, septal, ACG 7.43 59.8 Right
2167 Tumour Medial, polar 5.46 6.0 Right

NF
1049 Tumour Temporal (Left) NA 17.8 Right
1058 Stroke Parietal (Left) NA 3.5 Right
2028 Stroke Temporal, occipital (Left) 0.95 28.5 Right
2032 Lobectomy Temporal (Left) 1.60 49.6 Right
2036 Lobectomy Temporal (Left) NA 91.3 Right
2038 Lobectomy Temporal (Left) 1.17 144.7 Right
2040 Lobectomy Temporal (Right) 2.06 89.3 Right
2043 Stroke Occipital (Right) 0.48 36.3 Right
2054 Lobectomy Temporal (Left) NA 142.6 Right
2057 Lobectomy Temporal (Right) 2.66 134.6 Right
2103 Stroke Parietal, occipital (Right) 0.74 34.6 Right

*Percentage lesion size of total brain volume for certain patients varied across studies by a minimal amount due to re®nements in
measurement. The variations do not alter any group differences. **See caption for Fig. 1. ACG = anterior cingulate gyrus; NA = not
available.

(Knight et al., 1981; Woods and Knight, 1986; Alivisatos and To assess the effects of focal lesions on IIV, we used RT
Milner, 1989; Stuss et al., 1999) or as if sustaining control tasks designed to allow serial analyses of reaction times and
over distinctive criteria between targets and non-targets is lost errors moving from simple RT to increasingly more complex
(Stuss et al., 2002b). Lesions of the right frontal area have RT tasks, including the ability to analyse the effect of
been correlated with de®cits in a number of tasks requiring redundant information. Four different types of RT tasks were
sustained attention (Woods and Knight, 1986; Deutsch et al., administered (Stuss et al., 2002b). The theoretical framework
1987; Stuss et al., 1987; Wilkins et al., 1987; Glosser and for task design was detection using feature integration.
Goodglass, 1990). In summary, if focal lesions result in Complexity was de®ned by the type and number of features
increased IIV, there is considerable evidence to suggest the that had to be analysed. The higher level of task included the
importance of the frontal lesions, particularly on the right. mental operations of the previous task, plus an added process
This possibility has never been directly tested. (Donders, 1969; Sternberg, 1969). This task was selected
2366 D. T. Stuss et al.

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020

Fig. 1 Schematics of lesion location. The lesion location for the available scans for each patient in each
of the de®ned patient groups is illustrated. In some cases, lesion location had been documented and the
scan subsequently lost. As described in the text, the SM group is labelled superior medial, even though
several of the group had extension into IM regions, to distinguish them from the group with IM lesions only.

because it had been used effectively to study RT and dominant hand as quickly as possible, making as few errors as
variability in traumatic brain-injured individuals (Stuss et al., possible. In some of the tasks, a non-target stimulus was
1989, 1994b). In each task, the subject had to detect a target presented, requiring a response using a second response
stimulus and press a hand-held response button with the button mechanism held in the non-dominant hand.
Individual variability in reaction time 2367

Table 2 Sample sizes and mean demographic statistics for the two subject assessments
Sample Age Sex Education National Digit Boston Beck Lesion Time since
size (years) (proportion (years) adult reading span naming test depression size1 injury2
female) test forward inventory (months)

Single Assessment
LDL 6 53 0.67 12 100 4.5 37 4.7 1.6 62
RDL 7 57 0.29 10 102 5.3 52 1.2 2.8 10
SM 6 58 0.33 12 99 6.4 46 6.3 4.3 34
IM 6 46 0.17 11 100 6.0 47 4.2 1.4 20
NF 11 43 0.73 13 106 6.2 48 3.2 1.4 70

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


CTL 12 67 0.67 12 108 7.2 52 NA NA NA
Three repeated assessments
DL 6 61 0.40 10 101 5.3 48 3.8 2.2 56
SM 3 55 0.33 11 91 6.0 48 4.0 3.3 7.4
IM 4 55 0.25 9.3 99 6.3 50 3.5 1.6 20
NF 9 44 0.78 13 105 6.2 47 3.4 1.3 74
CTL 10 66 0.70 12 108 7.2 52 NA NA NA

Groups with frontal lesions are LDL, RDL, SM, IM and combined DL. Brackets indicate sample size where missing values occur. As
noted in the text, analyses were completed for the ®rst day of assessment (ONE), and for three separate test sessions approximately one
week apart (THREE). Because of attrition over the 3 weeks of testing, the patients with right or left lateral lesions were combined into
one group labelled DL. The sample sizes for the various groups are given in the ®rst column of the table. 1Size of lesion and TSI are
summarized from Table 1 to allow comparison of the groups in the single assessment and three repeated assessments. There are missing
values for some clinical variables. The size represents the percentage of lesion in relation to the total brain volume. 2TSI indicates the
chronicity of the lesion when the patient was entered into the study. NA = not applicable.

There were several hypotheses derived from the previous (iv) There was a CT or MRI scan demonstrating unequivo-
literature: cal frontal or NF damage.
(i) Patients with frontal lesions will show greater dispersion The exclusion criteria for patient subject selection were the
and inconsistency relative to control (CTL) group of partici- following: untreated hydrocephalus on CT or MRI scan;
pants and to patients with non-frontal (NF) lesions. presence of any systemic illness; history of alcoholism,
(ii) Based on previously demonstrated impairments in hospitalization for a psychiatric disorder, or prior neuro-
maintenance of sustained attention, patients with lesions of logical illness. The varied aetiologies allowed for the
the right frontal lobe will have impaired consistency of assessment of potential localization differences within the
performance; there is insuf®cient information in the literature frontal lobes (Stuss et al., 1995). In addition, the localization
to predict speci®c effects of other frontal lesion sites. of the lesion has been reported as more relevant than the
(iii) More complex RT tasks require more executive aetiology (Elsass and Hartelius, 1985; Stuss et al., 1994a;
control and, thus, in patients with lesions of the frontal lobes, Burgess and Shallice, 1996;).
such tasks will elicit greater IIV than simpler RT tasks. The patients were divided into ®ve groups based on the
(iv) We presume that the effects of errors on dispersion will location of their primary lesion. Eleven patients had path-
differ in the groups, but unique effects of different frontal ology located in NF regions (seven left, four right). They were
lesions are not speci®able. combined into one group for two reasons: posterior hemi-
spheric differences were not a focus of this study; and
preliminary analyses indicated no consistent differences on
Methods the tasks used between the left and right posterior lesioned
Subjects patients. The 25 patients with focal frontal lesions were
Thirty-six patients with focal lesions documented by CT or divided into four groups based on the location of their
MRI evidence were assessed. Inclusion criteria were as primary lesions: (i) left dorsolateral (LDL) frontal (n = 6); (ii)
follows: right dorsolateral (RDL) frontal (n = 7); (iii) inferior medial
(i) The aetiology was an acquired acute disorder such as (IM) (n = 6); and superior medial (SM) (n = 6). This
infarction, haemorrhage, trauma or resection of a benign classi®cation derived from a history of 10 years of uncovering
tumour; increasing anatomical/behavioural speci®city within the
(ii) There had been suf®cient time post-onset to allow for frontal lobes (for reviews see Stuss et al., 2002a; Stuss and
stability of the medical condition (range 1.3±291 months Levine, 2002). The patients classi®ed as SM tended to have
post-onset, mean = 42.4; all but one past 2.5 months); both IM and SM pathology. They were designated as SM to
(iii) Absence of severe aphasia or clinically detectable differentiate them from the patients who had IM pathology
neglect; only. The ®ve patient groups were compared with 12 control
2368 D. T. Stuss et al.

Table 3 Means and SDs of average reaction times (ii) Easy Choice RT (100 trials). Four different shapes were
LDL RDL IM SM NF Control presentedÐone designated as target (25% chance occur-
rence) and the other three as non-targets (75%).
Simple Mean 300 391 240 433 283 258 (iii) Complex RT (100 trials). The discrimination was
SD 61 220 15 145 55 45 based on three characteristics of the stimuliÐshape, colour,
Easy Mean 644 609 449 795 533 449
SD 230 193 45 193 124 63 and internal texture. The shapes appeared in one of four
Complex Mean 712 823 544 894 737 610 colours (yellow, green, blue and red) and contained internal
SD 143 210 62 131 182 135 texture in the form of lines that were oriented horizontally,
Redundant Mean 628 700 474 887 563 511 oriented vertically, slanting forward or slanting backward.
SD 149 341 68 251 165 116 The target, representing ~25% of the trials, was de®ned as a

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


particular combination of the three features (e.g. a red circle
with horizontal lines). The non-targets could be any other
combination of features.
subjects. The subjects were primarily right-handed. The (iv) Redundant RT (100 trials). In this task, the target was
presence of left-handed individuals were allowed in the characterized by a combination of three separate features, but
different patient groups for the following reasons: (i) the left subjects were informed about the fact that none of the non-
hander in the left brain damaged group was aphasic; (ii) the targets would contain any of the features in the target. That is,
left hander in the right brain damaged group was not aphasic if the target were a yellow square with backward slanting
and had a typical right hemisphere syndrome; and (iii) the lines, no other stimulus would be square, be coloured yellow,
third left hander was in the IM non-impaired group, where or have backward slanting lines. The Simple task was
laterality is not relevant. The lesion aetiology, location, lesion repeated after the Redundant task, but is not analysed here.
size, time since injury (TSI) (chronicity of lesion) and subject These tasks were presented in a ®xed order.
handedness are presented in Table 1. The individual lesions
divided by group are illustrated in Fig. 1.
The National Adult Reading Test, Digit Span forward, Measures of IIV/analyses of factors
Boston Naming Test, and Beck Depression Inventory were Mean RT and errors for the ®rst assessment have been
administered to all participants with a few exceptions. All presented elsewhere (Stuss et al., 2002b); the means and SDs
subjects had normal colour vision. Demographic and clinical for the RT results of this study are presented in Table 3 as
data are summarized for each of the groups in Table 2. The background information. In this paper, the focus is on
project was approved by the University of Toronto/Baycrest variation within an individual. There were two potential
Centre Human Subjects' Research Ethics Committee and categories of IIV studiedÐdispersion and consistency of
consent for participation in the project was obtained for each performance.
participant according to the Declaration of Helsinki.

Measures of dispersion
Dispersion refers to IIV within the continuous time period of
Tasks and procedures a single test. In our study, this was evaluated in the ®rst test
Stimuli measuring ~3 cm high and 3 cm wide were presented session. Each of the following scores was calculated for each
centrally on a 35 3 35 cm square colour monitor, located individual for each of the ®ve RT tasks.
~1 m from the subject's head position, at a variable inter-
stimulus interval lasting 4±6 s. Stimuli remained on the
screen until a response was made or for a default duration of Intra-individual standard deviation (ISD)
2 s. Subjects responded to a designated target stimulus by Within a task, we calculated the SD of each subject's RTs for
pressing the button on a hand-held response mechanism with correct target trials. The ISD provided a general index of each
their dominant hand. Non-target stimuli, when presented, subject's performance spread about his or her mean RT.
required a non-dominant hand response. Stimuli were always
one of four shapes (circle, square, triangle or cross). Subjects
were instructed to respond as quickly and as accurately as Intra-individual coef®cient of variation (ICV)
possible. To investigate the possibility that longer RTs could also be
There were four different RT tasks requiring different more variable for the sole reason that they are farther away
levels of feature discrimination and identi®cation; for more from the ¯oor, we calculated coef®cients of variation (ISD/
detailed explanations of the procedures, see Stuss et al. mean) for each subject. The ICV measures performance
1994b, 2002b). controlled to some degree for speed of response. To validate
(i) Simple RT (50 trials). A single shape, in light grey the use of the ICV, we also investigated the relationship
against the dark grey background of the computer screen, was between speed and variability within each group using a
presented; linear model of subject's SD in the Complex task as a
Individual variability in reaction time 2369

function of average RT, group membership, and the inter- the performance across the three sessions was compared for
action between RT and group. the following measures: mean RTs; number of errors; ISD;
ICV; autocorrelations; effects of errors; and trends.

Autocorrelation
For each subject's ®ve tests, correlation between consecutive
observations was calculated. This measure denoted how
Results
much linear association there was between one trial and the Demographic data
next. In patient studies where the emphasis is on lesion localiza-
tion, a variety of different abilities may occur in the different

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


patient subgroups for which it is dif®cult to ®nd controls. Our
major focus in selecting the CTL group was to control for
Factors possibly affecting dispersion
education and intelligence. There were no signi®cant differ-
Task complexity ences between any of the patient groups and the CTL group in
The effect of task complexity, as de®ned in these feature this regard. Other signi®cant demographic differences were
integration tasks, on dispersion was analysed by comparing observed. The age of the CTL group was signi®cantly older
the effect of increasing complexity of choice offered by the than the NF group [F(1,42) = 23, P < 0.0001], the IM group
Simple, Easy and Complex RT tasks. [F(1,42) = 13, P = 0.001] and the LDL group [F(1,42) = 5.2,
P = 0.03]. Forward digit span was signi®cantly shorter in the
RDL [F(1,33) = 8.4, P = 0.007] and LDL [F(1,33) = 7.7,
Speed of RT P = 0.009] groups relative to the CTL group. There were no
Since speed of RT has been related to increased variability differences among the patient groups on the Beck Depression
(Salthouse, 1993), we examined the relation of average RT to Inventory measureÐthe group means ranging from 1.2 to 6.3,
ISD. with no subject over 11. Among the patient groups, there was
a signi®cant difference in lesion size between the groups
[F(4,27) = 3.8, P = 0.01], with the SM group having the
Trends largest lesions.
Steadily changing RT would increase IIV. To see if there was For the comparison across the 3 days of testing, there
any linear drift in an individual's RT across the duration of a remained six dorsolateral frontal (DL) patients (two LDL,
task, we calculated the linear slope estimate for each subject's four RDL), four IM patients, three SM patients, nine NF
®ve tests. patients and 10 CTL participants. The DL group had a
signi®cantly shorter forward digit span [F(1,26) = 7.4,
P = 0.01] and the SM group had a signi®cantly lower
Errors National Adult Reading Test score [F(1,25) = 8.7, P = 0.007].
The presence of errors could be related to increased Demographic and neuropsychological variables showed
dispersion. We ®rst determined whether there was a general similar statistical differences for the IM and NF groups on
relationship between the number of errors and IIV. We then this reduced sample as in the full sampleÐexcept that the IM
examined the effect of errors on RT by calculating the group was no longer different on age [F(1,27) = 2.4, P = 0.13].
following: On this reduced sample, we found no effect of group on either
(i) The pre-error effect on RT, measured as the difference lesion size or time since injury. Table 2 summarizes the
between RT for the trial immediately preceding an error and demographic, neuropsychological and clinical characteristics
RT for the erroneous trial and calculated the average of these for the sample of subjects who participated in the three test
differences for each subject; sessions.
(ii) The post-error effect on RT, measured as the difference
between the RT for an erroneous trial and the RT for the
subsequent trial and averaged these differences for each Dispersion: ®rst test session
subject. ISD
ISD was calculated for each subject within each of the four
tasks (Simple, Easy, Complex and Redundant) and group
Consistency differences were investigated using simple contrasts between
Consistency of performance is de®ned as the ability of an each lesion group and the CTL group. As presented
individual to perform comparably across different testing graphically in Fig. 2, ISD was signi®cantly higher on the
sessions. Inconsistency indicates impairment in this ability. In Easy task for the SM [F(1,42) = 10, P = 0.003], RDL
this study, to assess IIV across non-continuous time periods, [F(1,42) = 7.4, P = 0.009) and LDL [F(1,42) = 7.1, P = 0.01]
the same tests were repeated on two additional occasionsÐall groups relative to the CTL. ISD was signi®cantly higher on
three testing sessions occurring ~1 week apart. For each test, the Complex task for the RDL [F(1,42) = 16, P = 0.0002], SM
2370 D. T. Stuss et al.

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


Fig. 2 Average ISD for the Simple, Easy, Complex and Redundant RT tasks.

[F(1,42) = 12, P = 0.001], LDL [F(1,42) = 5.9, P = 0.02] and day. ANOVA (analysis of variance) did not detect differences
NF [F(1,42) = 6.1, P = 0.02] groups relative to the CTL. ISD between patient groups and CTL group in their lag-1 auto-
was signi®cantly higher on the Redundant task for the SM correlation (P < 0.18).
[F(1,42) = 15, P = 0.0004] and LDL [F(1,42) = 8.0, P = 0.007]
groups relative to the CTL. The IM group did not show
signi®cantly elevated ISD on any of these tasks. Thus, using Factors affecting dispersion
the ISD measure of dispersion, all frontal groups except the Task complexity. Because of the reported relationship of IIV
IM group revealed greater ISD than the CTL. The NF group to task complexity, repeated measures ANOVA was evalu-
had signi®cantly greater ISD than the CTL only on the ated for the ISD across the Simple, Easy, Complex and
Complex task. Redundant tasks. As can be seen in Fig. 2, the pro®le across
the four tasks for the control group was different from the
pro®les for the LDL [F(3, 123) = 3.5, P = 0.02] and NF
[F(3, 123) = 3.2, P = 0.03] groups. Dispersion in the control
ICV group decreased from the Simple to the Easy task, whereas it
The ICV was calculated for each subject within each task and
increased in the LDL group. The NF group interaction was
group differences were investigated using contrasts to the
due to this group's large reduction in dispersion from
CTLs. The mean ICV for each group on each task is presented
Complex to Redundant tasks. When this same complexity
in Fig. 3. ICV was signi®cantly higher on the Easy task for the
evaluation was completed for ICV (see Fig. 3), no signi®cant
RDL [F(1,42) = 7.6, P = 0.009] and LDL [F(1,42) = 4.3,
differences between pro®les were observed.
P = 0.045] groups relative to the CTL. ICV was signi®cantly
higher on the Complex task for the RDL [F(1,42) = 11, Average RT. We investigated the relationship between an
p=.002], SM [F(1,42) = 5.3, P = 0.03] and LDL [F(1,42) = 5.1, individual's average RT time and their SD deviation to see
P = 0.03] groups relative to the CTL. ICV was signi®cantly how RT affected IIV. ISD was modelled as a function of
higher on the Redundant task for the LDL [F(1,42) = 6.6, group, average RT, and the interaction between group and
P = 0.01] group relative to the CTL. There were no signi®cant RT. Fig. 4 shows the slope estimates for each group's
ICV differences for the IM and NF groups. regression of ISD on average RT for the Complex task across
the range of individual average RT in each group and passing
through the group's grand average RT (the centre symbol on
Autocorrelation each regression line). There was little evidence for a
The correlation between RTs for adjacent trials was calcu- relationship between average RT and the ISD in most groups.
lated for each subject and for each task performed on the ®rst For example, the two medial (SM and IM) groups, the former
Individual variability in reaction time 2371

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


Fig. 3 Average ICV for the Simple, Easy, Complex, and Redundant RT tasks.

Fig. 4 Regression of ISD on mean RT. The symbol for each group locates average mean RT and average
ISD on that group's regression line. The slope of the regression line across the group's range indicates the
magnitude of the association between mean RT and ISD. The LDL group, with the third shortest average
mean RT showed a signi®cantly larger association between mean RT and ISD than the control group (CTL).

with notable IIV and the latter not, were most similar to the Trends. Slopes were calculated within each patient's con-
CTL group with respect to their relationship between tinuous stream of RTs for each task in an effort to detect any
variability and average RT. The LDL group, with the third consistent speeding up (negative slope) or slowing down
fastest mean RT, showed the largest association between ISD (positive slope) throughout the period that might affect any
and average RT (b = 0.60)Ða signi®cantly larger association dispersion measure. Only the two lateral groups revealed
than the CTLs [F(1,36) = 5.7, P = 0.02]. signi®cant slope differences compared with CTLs: the RDL
2372 D. T. Stuss et al.

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


Fig. 5 Regression of ISD on sensitivity. Propensity for making errors of any type (sensitivity) is measured
by d¢. The symbol for each group locates average d¢ and average ISD on that group's regression line. The
slope of the regression line across the group's range indicates the magnitude of the association between
sensitivity and ISD. Despite the differences in sensitivity between the RDL and LDL groups, both groups
show similar associations between ISD and sensitivity.

group on the Simple task, with a negative average slope average change in RT before and the average change in RT
signi®cantly different than the CTL group's average slope after an error. Fig. 6 shows the average RT on trials with an
[F(1,41) = 4.6, P = 0.04]; the LDL group on the Easy task, incorrect response for subjects within each group who made
with a positive average slope signi®cantly different than the at least one error. The average RT change from the correct
CTL group [F(1,42) = 6.1, P = 0.02], and on the Complex antecedent response to the erroneous response and the
task, with an average negative slope signi®cantly different average RT change from the erroneous response to the
than the CTL group [F(1,42) = 5.3, P = 0.03]. correct subsequent response are depicted with lines to the left
and right of the symbol identifying each group (acceleration
General effect of error rates. We examined whether com- with a negative slope and deceleration with a positive slope).
mitting errors in the Complex task was related to increased The normal pro®le is shorter RT on the error trials and longer
variability. As already described, the LDL, RDL, SM and NF RT on the trial after an error (Rabbitt and Vyas, 1970), as if
groups each had higher ISD than the CTL. In a previous paper recalibrating response speed. The IM group showed the
describing the basic RT data for this experiment (Stuss et al., expected pro®le before and after an error. Before an error, the
2002b), the RDL group alone had a signi®cantly lower SM group revealed slowing (although not signi®cant,
sensitivity measure (d¢) than the CTL group; i.e. they were P = 0.13) on the erroneous trial. Three groups (IM, NF and
impaired in discriminating targets from non-targets. In Fig. 5, control) showed the expected slowing after an error. The RDL
average ISD and average d¢ scores on the Complex task are group was somewhat ¯at before and after an error. The LDL
plotted with the symbols for each group, and the slope of the group on average was 174 ms faster on trials after an error,
effect of d¢ on ISD for each group is illustrated with a which was signi®cantly different from the control group
regression line across the groups' ranges. The two medial [F(1,35) = 5.0, P = 0.03].
(SM, IM) and NF groups were not signi®cantly different from
the CTL. The RDL group showed a negative association
between d¢ and ISD, which was signi®cantly different from Summary
the CTL group [F(1,36) = 4.3, P = 0.045]. The next largest Dispersion was assessed for the ®rst test session allowing the
association was in the LDL group. full sample of participants to be included. All groups of
frontal patients (except the IM group) had greater dispersion
Local effect of errors. Two RT differences were calculated in than the CTL. The NF group was signi®cantly different from
the Complex task, where the most errors occurred: the the CTL only on the Complex task, and only for ISD.
Individual variability in reaction time 2373

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


Fig. 6 Relationship in RT speed for trials antecedent and subsequent to an error. The symbol for each
group locates average RT for trials with an erroneous response. Direction and magnitude of changes in
RT antecedent and subsequent to an error are identi®ed by the slope of the lines to the left and right of
each group's symbol. A positively sloped line indicates slowing while a negatively sloped line indicates
acceleration. The control group followed the normal pattern (Rabbit and Vyas, 1970) of speeding up into
an error and slowing after. Note the slowing from the antecedent to the error trial in the SM group and
the acceleration after error trials in the LDL group. The RDL group revealed little ¯uctuation before or
after an error.

Different factors increased IIV in different lesion groups inconsistent on at least one measure of dispersion (ISD or
relative to CTL group. Increasing task complexity by adding ICV) than the CTL group on the Easy [ISD, F(1,26) = 7.6,
a choice component to the reaction time affected ISD in the P = 0.01; ICV, F(1,26) = 2.0, P = 0.17], Complex [ISD,
LDL and NF groups. An overall slow response time was F(1,27) = 5.9, P = 0.02; ICV, F(1,27) = 11, P = 0.003] and
associated with increased ISD in the LDL group. The LDL Redundant [ISD, F(1,27) = 5.6, P = 0.03; ICV, F(1,27) = 4.4,
group was markedly faster on the trial after an error. An P = 0.046] tasks. The SM group was more inconsistent
increase in error rate was associated with markedly increased in dispersion (ISD and ICV) than the CTL on the
IIV in the RDL group. Redundant task only [ISD, F(1,27) = 24, P < 0.0001; ICV,
F(1,31) = 5.4, P = 0.03]. The NF group was more inconsistent
in dispersion relative to the CTL on the Complex task [ISD,
Consistency across test sessions F(1,27) = 3.8, P = 0.06; ICV, F(1,27) = 6.5, P = 0.02]. Again,
inconsistency in the IM group was not signi®cantly different
Inconsistency of mean RT from the CTL.
The ®rst analysis compared the changes in mean RT over the
3 days. The DL group was more inconsistent in mean
performance than the CTL group on the Simple [F(1,26) = 4.5,
P = 0.04), Easy [F(1,26) = 7.0, P = 0.01), and Redundant The redundancy effect
[F(1,27) = 8.2, P = 0.008) tasks. The SM group was The Easy and Redundant tasks do not differ in actual
signi®cantly more inconsistent than the CTL on the dif®culty even though the presence of three features in the
Redundant task [F(1,27) = 5.1, P = 0.03]. Inconsistency for Redundant task stimuli suggests an apparently greater
the IM and NF groups did not differ from the CTL. complexity. Comparison of the Easy and Redundant tasks
provides an index of the effect of irrelevant information in a
stimulus. The difference between a subject's speed on the
Inconsistency of ISD and ICV Redundant and Easy tasks was more variable over the three
These are described together since the results are almost assessment sessions for patients in the DL group relative to
identical for the two measures. The DL group was more the CTL group [F(1,31) = 13, P = 0.001].
2374 D. T. Stuss et al.

Errors (iii) There are different kinds of IIV. Not all types are
In a previous paper examining the RT and errors of the same elevated as a consequence of brain damage and different
patients on these tasks (Stuss et al., 2002b), we reported that types of IIV are affected by damage in different brain regions.
the LDL group had decreased response bias (c)Ðtended to If disorders of stability of performance re¯ect impairment in
make primarily false positive errorsÐpresumably a criterion top±down control, multiple mechanisms of control are
setting problem. The RDL group, on the other hand, had disturbed.
decreased response sensitivity (d¢)Ðmade more errors of all (iv) Task factors have important effects on demonstration
typesÐpresumably a problem differentiating targets and non- of variability.
targets. The SM group exhibited an error pattern, in terms of
bias and sensitivity, which fell in between the LDL and RDL

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


groups. In this paper, we analysed whether bias and
sensitivity changed over the three testing days. With the Lesion site effects
groups as de®ned, there were no signi®cant differences from IIV on RT tasks is signi®cantly increased in most patients
CTL subjects on any task on either d¢ or bias (NF, d¢, with frontal injury, but the effects are not uniform across all
complex, P > 0.06). Because of the potential importance of frontal regions.
the regional differences within the frontal lobes (which by Dispersion was highly associated with frontal injury (with
grouping both DL groups may have obscured any ®ndings), the exception of the IM group) and was abnormal in the NF
we also analysed the original groups, even though the sample patients on the tests used here only for the Complex task ISD
size was reduced. No group had signi®cantly different measurement. Thus, increased dispersion on RT tasks,
inconsistency of sensitivity or bias compared with the CTL measured by both ISD and ICV, is clearly more affected by
group. That is, the group impairment in bias (LDL) or SM and DL frontal lesions, even at a level of simple feature
sensitivity (RDL) was consistent from test session to test discrimination and choice. Dispersion is not a general effect
session. of any brain damage, although task context may play a role
(see below).
Analysis of lesion site effects on inconsistency could not be
Summary examined in such detail because of sample attrition secondary
Consistency of performance was assessed by comparison of to the demands of three consecutive weeks of testing (see
measures over three assessment days. The consistency below). All of the patient groups, except the IM group, had
®ndings were interpreted compared with consistency in the
some degree of inconsistency.
CTL group. Normal consistency means that performance on
Task demands are likely to have an effect on whether IIV is
one testing session on a given measure will as closely re¯ect
observed or not after lesions in different regions. For
performance on another testing session as the same compari-
example, the IM group revealed no IIV in the RT tasks
son in the CTL group. There could be (and was) abnormal
used. Yet, in a study on the Wisconsin Card Sorting Test, this
dispersion within a test session, but the dispersion could be
same group had dif®culty staying on task (and thus were
(and often was) consistent between different test sessions.
variable in a certain manner) under certain task conditions
Dispersion and inconsistency are different measures of IIV.
and not others (Stuss et al., 2000). The NF patients were
The IM group did not show any inconsistency in perform-
variable when the task required three feature integration, such
ance. All other patient groups were inconsistent on many
measures. The lateral (LDL, RDL) and SM frontal groups integration having been related to posterior brain regions
were inconsistent on considerably more measures than the NF (Bernstein and Robertson, 1998). There has been reported IIV
group. after right and left brain injury related to neglect and lexical
decision tasks, respectively (Anderson et al., 2000; Milberg
et al., 2003). In future research, the potential impact of any
frontal involvement in the patients examined, the differential
Discussion impact of speci®c task demands (e.g. feature integration,
There are four main conclusions from our study: visual spatial attention, language), general task complexity
(i) Increased IIV may be caused by damage to speci®c and the possible interactions of these factors should be
brain regions. Lesions in the frontal lobes (with the exception investigated.
of the ventral medial/orbitofrontal region) in particular impair
stability of behaviour and led to increased IIV on the tests
used here.
(ii) These ¯uctuations of performance in an individual are Lesion and test factors affecting variability
not simply error variance or statistical noise (Kelly et al., The effects of frontal lesions on IIV are complicated by
2001). Individual differences, inter-trial ¯uctuations and interactions between lesion site and task factors, and the
inconsistency over repeated assessments are important results of this study illuminate some of the reasons for
measures of impairment. con¯icting results in past reports.
Individual variability in reaction time 2375

Relationship between average performance and For the right lateral frontal group, an increase in the error rate
variability was associated with increased dispersion (ISD). Analysis of
To investigate the impact of average performance on IIV, the RT pre- and post-errors as an index of executive control
ICV was used as one way of adjusting for the mean reveals a complex pattern: the RDL group was not abnor-
performance of the individual, and then comparing ISD and mally affected by an error; the LDL group was faster after an
ICV results. A comparison of the ISD and ICV results across error; and the SM group was much slower on trials with an
all tasks illustrated that dispersion measured as ISD was no error than the preceding trial. Different frontal regions
longer signi®cant when measured as ICV in the following contribute different mechanisms of control to the RT target
cases: Easy RT: SM group; Complex RT: NF group; behaviour.

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


Redundant RT: SM group. Note that the SM group had the
slowest RT and the LDL group among the faster.
A direct method of analysing the relationship between IIV Consistency versus dispersion
and average performance is to compare the slope of ISD with We tested a subset of the patients on three separate occasions
respect to average performance within each group compared over 3 weeks. All of the patient groups (excepting IM) had
with the CTL. Only the LDL group was signi®cantly different greater inconsistency, but the DL frontal patients were
from the CTL in its association between individual variability particularly inconsistent. The DL patients showed greater
and average RT. The SM group, with the slowest RT, showed inconsistency than the CTL, had more instances of inconsist-
the ¯attest relationship between ISD and performance, second ency than the NF group, and only patients with DL frontal
only to the CTL. pathology were inconsistent dealing with extraneous infor-
There have been con¯icting reports about the relationship mation on the Redundant RT task. Three assessments may not
between variability and mean performance, particularly in RT have been suf®cient (especially with small groups) to uncover
tasks. Some claim a direct relationship between mean RT and details about inconsistency, although Spikman et al. (1996),
both diversity and dispersion (Hale et al., 1988; Salthouse, who reported increased IIV after TBI, noted that IIV actually
1993); others demonstrate the relative independence of IIV diminished by the fourth block of testing. Consistency
from RT latency (Schwartz et al., 1989; Whyte et al., 1995; appears more robust than dispersion, in that it was not as
West et al., 2002b). Our results using the RT tasks in this affected by lesions as dispersion, but the investigation of
study do not support a necessary relationship between an consistency of performance is just beginning.
individual's lengthening of RT and individual variability.

Unaffected aspects of variability


Not all indices of IIV are affected by brain damage. We did
Specifying complexity not ®nd signi®cant group differences in consecutive trial
This is not transparent. In our study, the signi®cant effects of
¯uctuations, as assessed by autocorrelations. This measure
complexity were seen in the comparison of Simple to Easy
denoted how much linear association there was between one
tasks in the LDL group only, with no additional effect into the
trial and the next. We used autocorrelations to investigate trial
Complex task. The step from constant stimulus±response
to trial patterns rather than autocovariance because the former
mapping to any level of variable response appeared suf®cient
adjusts for inter-trial variability (Wei, 1990). That is, while
to elicit greater IIV in this susceptible patient group. In
the actual RTs among the groups may have differed, the
patients with left frontal injury, if the executive control
¯uctuations from trial-to-trial of individuals regardless of
system is already stressed, little complexity is required to
group were as stable as the CTL group.
produce failure of top±down control. In normal individuals,
for a task to be complex enough to stress the executive control
system, it must be much more dif®cult (West, 1999a).
Regional brain lesions and variability
Our ®rst hypothesis was supported. Patients with frontal
lesions do have greater IIV on these RT tasks than CTL
Trends subjects or patients with NF lesions, but the increased IIV is
Only the lateral groups showed signi®cant differences in not seen uniformly. Patients with IM lesions have absolutely
trendsÐthe tendency to speed up or slow down over time. normal levels of IIV on the tasks used. The abnormal
Drift will affect ISD and ICV. The fact that the SM group did dispersion on ISD, which is not present with ICV, and only
not show signi®cantly different slope suggests that several the occasional appearance of inconsistency in the posterior
different factors may affect ISD and ICV in different groups. lesion group, who were comparable statistically with the CTL
in most measures, indicates that increased IIV is not simply
due to brain damage. To the best of our knowledge, our
Errors results (®rst presented in Stuss et al., 1999) are the ®rst
There are effects of both the overall rate of errors and of the demonstration of a focal CNS cause of abnormal intra-
immediate neighbourhood presence of an error on dispersion. individual variation. IIV is modulated by stimulus±response
2376 D. T. Stuss et al.

control mechanisms (Rabbitt and Rodgers, 1977); and those utilization (Konow and Pribram, 1970), as if attention were
control mechanisms for the execution of behaviours/ captured by the error. A seemingly similar and selective LDL
responses are largely located in the frontal lobes. Whether frontal de®cit was reported in our earlier study (Stuss et al.,
this level of control is unique to the frontal lobes remains to 1999) using an Inhibition of Return paradigm. The left frontal
be fully determined. However, in those studies that have group in that study showed facilitation rather than inhibition
demonstrated IIV after right or left hemisphere lesions, there of return.
is a need to dissociate the differential impact of frontal versus The SM group was slower on trials with an error, but after
non-frontal involvement, and the relationship of the task the error, there was no additional slowing. This result
demands (e.g. language) to the location of the lesion. It is suggests that the patients in the SM group were alerted by
possible that content-related variability may be more domain- committing an error. We have proposed that the fundamental

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


speci®c and related to NF regions, with the frontal lobes impairment caused by damage to the SM areas is maintaining
contributing a more generic top±down control. response activation or energization. We have demonstrated
The second hypothesis was partly supported. Patients with blunted activation in this group on numerous tasks: the Stroop
right frontal lesions do have increased inconsistency, but so test (Stuss et al., 2001), verbal ¯uency (Stuss et al., 1998) and
do the LDL and SM groups. The patients with lateral frontal Simple RT (Stuss et al., 2002b). The current error feedback
regions may have a particular propensity to be affected by results strongly support this view. SM damage causes loss of
inconsistency of performance. The potential laterality and activation over time and RT becomes slower. Then, with an
mechanisms of these effects need to be studied with a larger external warning stimulus (the error), arousal or effort
number of patients. The third hypothesis, that increased necessary to maintain that level of activation is restoredÐat
complexity would increase IIV in patients with frontal least temporarily. In clinical reports. this behaviour has been
lesions, was supported and in an intriguing, not altogether labelled `drifting attention' (Stuss and Benson, 1986).
expected, manner. No signi®cant differences were found for
either ISD or ICV in the Simple RT task, but signi®cant
differences were observed for the Easy task for all except the A tentative model: effects of speci®c frontal
IM and NF groups. The critical step was introducing any lesions on IIV
complexity, i.e. going from Simple to Easy choice. When the Lesions in the SM region disrupt maintenance of activation to
effect of complexity was examined directly, the increased respond and of energization of various schemata in the
dispersion from the Simple to Easy tasks was observed in the response set (see also Stuss et al., 1995). Thus, lesions in the
LDL group. The fourth hypothesis was under-speci®ed: a SM region cause signi®cant dispersion and inconsistency
general presumption that errors would have a different effect compared with CTLs that is not simply due to errors or speed,
on IIV in patients with frontal lesions than in CTLs. Although even though this group was the slowest of the patient groups.
weak, the hypothesis was supported. Error feedback is one Lesions in the RDL region impair sensitivityÐthe ability
index of the control mechanism. If error analysis can be to differentiate the correct stimulus. Thus, patients with RDL
considered an indirect re¯ection of control mechanisms, this lesions make multiple errors and, in this group, it is the
study demonstrates different disorders of control related to overall error rate that is associated with IIV. The effect of a
lesion location within the frontal lobes. Normal subjects particular error on the surrounding trials is weak as the
maintain fast and accurate responses by dynamic response patients are relatively insensitive to errors.
programming: error responses tend to be faster than correct Lesions in the LDL region impair establishment of criteria
responses, but after error detection responses slow as if re- for functional response. Thus, dispersion is high, and
calibrating speed-accuracy limitations (Rabbitt and Vyas, complexity and, probably to some degree errors and
1970). To a greater or lesser degree, the CTL, IM frontal and inconsistent bias, all combine to increase IIV. This was the
NF groups exhibited this normal pro®le of response tracking one group in which the RT slowing was related to variability,
with faster responses preceding errors, followed by slowing. even though this group was among the faster patient groups.
The RT of the RDL group was least affected by or after an The IM group had normal IIV. If variability is related to
error. This is compatible with our previous report (Stuss et al., executive control of the deployment of attentional resources,
2002b) that this group showed the greatest impairment in of activation to respond and to maintenance of sharp criteria
sensitivityÐde®ned as the ability to differentiate ef®ciently (`if-then' operations) as in our earlier model (Stuss et al,
between targets and non-targets. Patients with RDL lesions 1995), then IM regions apparently do not contribute to this
have dif®culty distinguishing what is important, and their deployment. On a much different task, the Wisconsin Card
lack of differential reaction to errors indicates low sensitivity Sorting Test (Stuss et al., 2001), when patients in the IM
to target. Low sensitivity and absence of change in response lesion group were made explicitly aware of their on-going
time after errors may underlie monitoring de®cits after right performance, theyÐuniquely among frontal injured pa-
frontal injury. In contrast to the CTL group, the LDL group tientsÐappeared to lose track of what they were doing.
had faster reaction times after the error. This suggests a de®cit This may be a different type of variability of performance at
not in error detection (which would be re¯ected in minimal or the level of simultaneous attention to accuracy and to
no difference in RT as in the RDL group), but in error feedback.
Individual variability in reaction time 2377

The model that we propose requires several caveats. To we demonstrated that there were no consistent changes in the
insure that the basic RT task could be performed at a high slope of performance over time. It may be that the ¯uctuating
level, we excluded patients with signi®cant aphasia or `top±down' attention that we have reported is a partial
neglect. When a task has high verbal demands, there may explanation for impaired sustained attention in some groups
be high IIV introduced by aphasia. When a task has high rather than the opposite. With regard to working memory, the
perceptual demands, visual neglect may inject IIV. Increased tasks have low demands on working memory as they are
IIV on domain-speci®c tasks is likely with lesions that disrupt blocked, require no response shift demands during blocks, and
performance within those domains and has been demon- show no consistent relationship between potential complexity
strated for spatial neglect. Our results cannot be reduced to that might increase `keeping in mind' burdens. With regard to
differences in demographic variables, although these may perseveration and failure to inhibit responses, these terms are

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


have some effect. For example, simple attentional problems surface descriptions of error types more than basic processes.
cannot explain the patterns of group differences. The LDL Our patients made errors of these types, but there was no
and the RDL groups had lower forward digit span, but not the consistent relationship between errors and IIV except in the
SM group. Since these are the three groups which displayed RDL group. There may be multiple routes to perseveration
the most variability, it is unlikely that digit span scores were a and failure to inhibit depending on task, and we have
primary contributor to IIV. Age differences from the CTL demonstrated this in other studies (Stuss et al., 1999, 2000).
group were observed for NF, IM and LDL groups, of which With regard to strategy formation, patients with left DL and
the former two were not variable. Differences in education or right DL lesions surely do have impairments in strategy
intelligence are not likely to have a major impact, as there formulation. In this and other reports (Stuss et al., 1994a,
were no signi®cant differences between the CTL group and 2002b; Alexander et al., 2003), we have demonstrated that
any of the patient groups for the dispersion measures. patients with left DL lesions adopt a strategy of shifted bias
Secondly, we are also aware and have published on the and that patients with right DL lesions adopt a strategy of
possible effect of time of day on variability (West et al., reduced sensitivity. Those strategies account for the nature of
2002a). Our subjects were studied at different times of the their errors, but not the variability in their correct responses.
day, depending on their availability but there was no In this experiment, only the redundant task offers the
systematic bias across groups. However, for the repeated possibility of creating a strategy during the stimulus presen-
testings, time of day was kept constant for the individual tations, that is, once the redundancy is detected. There may
subjectÐthus controlling for that factor within each partici- have been an interaction between strategy and variability in
pant for the consistency measures. that task.
A third caveat concerns the distinction between frontal Rather than account for `micro-behaviours' such as
lobe lesions and frontal system lesions. This report focused on ¯uctuating attention with `macro-behaviours' such as perse-
patients with focal frontal lobe lesions, but there are extensive veration or inhibition failure, we prefer to demonstrate a
cortico-cortical and frontal-subcortical connections (e.g. range of micro-behaviours that, depending upon varied and
Nauta, 1971, 1973; Wiesendanger and Wise, 1992; Petrides distinctive patterns of recruitment, add up to the various
and Pandya, 1994, 1999) that may support performance macro-behaviours. In the original outline (Stuss et al., 1995)
capacities. Damage to focal frontal regions or to NF regions of this modi®ed form of the Norman and Shallice (1986)
such as basal ganglia (Cummings, 1993) or cerebellum theory, we proposed a number of forms of attention, all under
(Holmes, 1939; Bastian et al., 1996) may produce similar the control of frontal structures, which are differentially
de®cits in executive function. A similar proposal of `frontal recruited under different cognitive contexts to produce the
lobe' dysfunction has been made for the increased IIV coarser behaviours that are commonly considered `frontal
reported in normal elderly people (West, 1999b; West et al., lobe functions'.
2002b). Frontal lobe dysfunction has also been proposed to
account for the increased IIV noted in TBI (thought to affect
the integrity of the frontal lobes) individuals (Stuss et al., Clinical implications
1989, 1994b). There is a very signi®cant implication of these data. A
A fourth caveat is the fundamental claim that there are patient's mean performance at one time may not re¯ect wide
properties of top±down regulation of attention that are irregularities over time and thus a single clinical assessment
instantiated in frontal structures (and their connections). of a patient with a frontal lesion may not capture dispersion or
There is a litany of impairments associated with frontal injury inconsistency. Success in real-life tasks may depend as much
that might be recruited to account for our ®ndings: reduced on predictability and consistency as on average performance.
sustained attention; poor working memory; perseveration; Can dispersion and inconsistency be reduced? Bleiberg
failure to inhibit responses; and poor action planning or et al. (1993) administered dextroamphetamine in a single
strategy formulation. It is likely that some of these putative subject placebo crossover design to an individual with TBI.
de®cits do play a role in overall performance, but none seems On treatment only, variability decreased, but only the SDs
adequate to account for the general results on RT or to the were reported, so the relationship to overall RT speed is
speci®c ®ndings for IIV. With regard to sustained attention, unknown. Verbal self-regulation (Luria, 1966) may be
2378 D. T. Stuss et al.

effective for tasks that unfold at a slower pace than RT tasks. Barratt ES. Intra-individual variability of performance: ANS and
It was successful in reducing motor impersistenceÐa psychometric correlates. Tex Rep Biol Med 1963; 21: 496±504.
disorder most commonly found after focal right frontal Bastian AJ, Martin TA, Keating JG, Thach WT. Cerebellar ataxia:
pathology that has some similarity to IIV (Stuss et al., 1987). abnormal control of interaction torques across multiple joints. J
The results of this study suggest a method to develop Neurophysiol 1996; 76: 492±509.
behavioural interventions: specify a patient's lesion location
Benton AL, Blackburn HL. Practice effects in reaction-time tasks in
with appropriate imaging, then identify the systems involved
brain-injured patients. J Abnorm Soc Psychol 1957; 54: 109±13.
(i.e. SM or left dorsolateral, etc.), then assess the speci®c
form of IIV through appropriate assessment. Patients with Bernstein LJ, Robertson LC. Illusory conjunctions of color and
injury in SM regions and the pro®le of variability demon- motion with shape following bilateral parietal lesions. Psychol Sci

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


strated here might respond to alerting cues to maintain 1998; 9: 167±75.
appropriate activation. Patients with RDL lesions might Bleiberg J, Garmoe W, Cederquist J, Reeves D, Lux W. Effects of
utilize explicit feedback to monitor their performance by dexedrine on performance consistency following brain injury.
distinguishing better between targets and non-targets. Neuropsychiatry Neuropsychol Behav Neurol 1993; 6: 245±248.
Clarifying the relationship between speci®c lesion sites and Bleiberg J, Garmoe WS, Halpern EL, Reeves DL, Nadler JD.
speci®c basic processes of attention should lead to more Consistency of within-day and across-day performance after mild
speci®c rehabilitation procedures and provide a base for brain injury. Neuropsychiatry Neuropsychol Behav Neurol 1997;
research efforts in rehabilitation. 10: 247±53.
Bleiberg J, Halpern EL, Reeves D, Daniel JC. Future directions for
the neuropsychological assessment of sports concussion. J Head
Acknowledgements Trauma Rehabil 1998; 13: 36±44.
We wish to thank the subjects for their participation and the
Bruhn P, Parsons OA. Continuous reaction time in brain damage.
following people for testing as well as for ®gure and
Cortex 1971; 7: 278±91.
manuscript preparation: S. Bisschop, A. Borowiec, L.
Buckle, R. Dempster, D. Derkzen, N. Fansabedian, D. Burgess PW, Shallice T. Response suppression, initiation and
Floden, D. Franchi, S. Gillingham, L. Hamer and A. Savas. strategy use following frontal lobe lesions. Neuropsychologia 1996;
R. West provided important feedback on earlier drafts. 34: 263±72.
Preliminary results of this study were ®rst presented at the Collins LF, Long CJ. Visual reaction time and its relationship to
27th Conference of the International Neuropsychological neuropsychological test performance. Arch Clin Neuropsychol
Society, Boston, MA, 1999, and published as an abstract 1996; 11: 613±23.
(Stuss et al., 1999). Funding for the research was provided by Cronbach LJ. The two disciplines of scienti®c psychology. Am
the Canadian Institute for Health Research (MT-12853; and Psychol 1957; 12: 671±84.
CIHR-14974). D. Stuss is the Reva James Leeds Chair in
Neuroscience and Research Leadership, Baycrest Centre and Cummings JL. Fronto-subcortical circuits and human behavior.
University of Toronto. Arch Neurol 1993; 50: 873±80.
Deutsch G, Papanicolaou AC, Bourbon WT, Eisenberg HM.
Cerebral blood ¯ow evidence of right frontal activation in
References attention demanding tasks. Int J Neurosci 1987; 36: 23±8.
Alexander MP, Stuss DT, Fansabedian N. California verbal learning Donders FC. On the speed of mental processes. Acta Psychol
test: performance by patients with focal frontal and non-frontal (Amst) 1969; 30: 412±31.
lesions. Brain 2003; 126: 1493±1503.
Elsass P, Hartelius H. Reaction time and brain disease: relations to
Alivisatos B, Milner B. Effects of frontal or temporal lobectomy on location, aetiology and progression of cerebral dysfunction. Acta
the use of advance information in a choice reaction time task. Neurol Scand 1985; 71: 11±19.
Neuropsychologia 1989; 27: 495±503.
Fink GR, Halligan PW, Marshall JC, Frith CD, Frackowiak RSJ,
Anderson B, Mennemeier M, Chatterjee A. Variability not ability: Dolan RJ. Neural mechanisms involved in the processing of global
another basis for performance decrements in neglect. Neuro- and local aspects of hierarchically organized visual stimuli. Brain
psychologia 2000; 38: 785±96. 1997; 120: 1779±91.
Anstey KJ. Sensorimotor variables and forced expiratory volume as Fiske DW, Rice L. Intra-individual response variability. Psychol
correlates of speed, accuracy, and variability in reaction time Bull 1955; 52: 217±50.
performance in late adulthood. Aging Neuropsychol C 1999; 6: 84±
95. Flugel JC. Practice, fatigue and oscillation. Br J Psychol Mono
Suppl 1928; 4: 1±92.
Ballard C, Walker M, O'Brien J, Rowan E, McKeith I. The
characterization and impact of `¯uctuating' cognition in dementia Foster JK, Behrmann M, Stuss DT. Aging and visual search:
with Lewy bodies and Alzheimer's disease. Int J Geriatr Psychiatry generalized cognitive slowing or selective de®cit in attention?
2001; 16: 494±98. Aging Cogn 1995; 2: 279±99.
Individual variability in reaction time 2379

Fozard JL, Vercruyssen M, Reynolds SL, Hancock PA, Quilter RE. In: Laitinen LV, Livingston KE, editors. Surgical approaches in
Age differences and changes in reaction time: The Baltimore psychiatry. Baltimore: University Park Press; 1973. p. 303±14.
Longitudinal Study of Aging. J Gerontol Psychol Sci 1994; 49:
Norman DA, Shallice T. Attention to action: willed and automatic
179±89.
control of behaviour. In: Davidson RJ, Schwartz GE, Shapiro D,
Glosser G, Goodglass H. Disorders in executive control functions editors. Consciousness and self-regulation: advances in research and
among aphasic and other brain-damaged patients. J Clin Exp theory, Vol. 4. New York: Plenum;1986. p. 1±18.
Neuropsychol 1990; 12: 485±501. Petrides M, Pandya DN. Comparative architectonic analysis of the
Goldstein K. After effects of brain injuries in war. New York: human and macaque frontal cortex. In: Boller F, Grafman J, editors.
Grune and Stratton; 1942. Handbook of neuropsychology, Vol. 9. Amsterdam: Elsevier; 1994.
p. 17±58.

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


Hale S, Myerson J, Smith GA, Poon LW. Age, variability, and
speed: between-subjects diversity. Psychol Aging 1988; 3: 407±10. Petrides M, Pandya DN. Dorsolateral prefrontal cortex: comparative
cytoarchitectonic analysis in the human and the macaque brain and
Head H. Aphasia and kindred disorders of speech. Cambridge: corticocortical connection pattterns. Eur J Neurosci 1999; 11: 1011±36.
University Press; 1926.
Philpott SJF. Fluctuations in human output. Br J Psyhol Mono
Hetherington CR, Stuss DT, Finlayson MAJ. Reaction time and Suppl 1933; 17: 6.
variability 5 and 10 years after traumatic brain injury. Brain Inj
1996; 10: 473±86. Rabbitt P, Rodgers B. What does a man do after he makes an error?
An analysis of response programming. Q J Exp Psychol 1977; 29:
Holmes G. The cerebellum of man. The Hughlings Jackson 727±43.
memorial lecture. Brain 1939; 62: 1±30.
Rabbitt PMA, Vyas SM. An elementary preliminary taxonomy for
Hultsch DF, MacDonald SWS, Hunter MA, Levy-Bencheton J, some errors in laboratory choice RT tasks. Acta Psychol (Amst)
Strauss E. Intraindividual variability in cognitive performance in 1970; 33: 56±76.
older adults: comparison of adults with mild dementia, adults with
Salthouse TA. Attentional blocks are not responsible for age-related
arthritis, and healthy adults. Neuropsychology 2000; 14: 588±98.
slowing. J Gerontol 1993; 48: 263±70.
Kelly A, Heathcote A, Heath R, Longstaff M. Response-time
Salthouse TA. The processing-speed theory of adult age differences
dynamics: evidence for linear and low-dimensional nonlinear
in cognition. Psychol Rev 1996; 103: 403±28.
structure in human choice sequences. Q J Exp Psychol A 2001;
54: 805±40. Schwartz F, Carr AC, Munich RL, Glauber S, Lesser B, Murray J.
Reaction-time impairment in schizophrenia and affective illness:
Knight RT, Hillyard SA, Woods DL, Neville HJ. The effects of
the role of attention. Biol Psychiatry 1989; 25: 540±8.
frontal cortex lesions on event-related potentials during auditory
selective attention. Electroencephalogr Clin Neurophysiol 1981; 52: Segalowitz SJ, Dywan J, Unsal A. Attentional factors in response
571±82. time variability after traumatic brain injury: an ERP study. J Int
Neuropsychol Soc 1997; 3: 95±107.
Konow A, Pribram KH. Error recognition and utilization produced
by injury to the frontal cortex in man. Neuropsychologia 1970; 8: Shammi P, Bosman E, Stuss DT. Aging and variability in
489±91. performance. Aging Neuropsychol Cogn 1998; 5: 1±13.

Leth-Steensen C, Elbaz ZK, Douglas VI. Mean response times, Spikman JM, van Zomeren AH, Deelman BG. De®cits of attention
variability, and skew in the responding of ADHD children: a after closed-head injury: slowness only? J Clin Exp Neuropsychol
response time distributional approach. Acta Psychol (Amst) 2000; 1996; 18: 755±67.
104: 167±90. Sternberg S. Memory scanning: mental processes revealed by
Lindenberger U, Baltes PB. Intellectual functioning in old and very reaction-time experiments. Am Sci 1969; 57: 421±57.
old age: cross-sectional results from the Berlin Aging Study. Stuss DT. Interference effects on memory functions in
Psychol Aging 1997; 12: 410±32. postleukotomy patients: an attentional perspective. In: Levin HS,
Luria AR. Higher cortical functions in man. New York: Basic Eisenberg HM, Benton AL, editors. Frontal lobe function and
Books; 1966. dysfunction. New York: Oxford University Press; 1991. p. 157±72.

Milberg WM, Blumstein S, Giovanello KS, Misiurski C. Stuss DT, Benson DF. The frontal lobes. New York: Raven Press; 1986.
Summation priming in aphasia: Evidence for alterations in Stuss DT, Levine B. Adult clinical neuropsychology: lessons from
semantic integration and activation. Brain Cogn 2003; 51: 31±47. studies of the frontal lobes. Annu Rev Psychol 2002; 53: 401±33.
Murtha S, Cismaru R, Waechter R, Chertkow H. Increased Stuss DT, Delgado M, Guzman DA. Verbal regulation in the control
variability accompanies frontal lobe damage in dementia. J Int of motor impersistence: a proposed rehabilitation procedure. J
Neuropsychol Soc 2002; 8: 360±72. Neurol Rehabil 1987; 1: 19±24.
Nauta WJH. The problem of the frontal lobe: a reinterpretation. J Stuss DT, Stethem LL, Hugenholtz H, Picton T, Pivik J, Richard
Psychiatr Res 1971; 8: 167±87. MT. Reaction time after head injury: fatigue, divided and focused
attention, and consistency of performance. J Neurol Neurosurg
Nauta WJH. Connections of the frontal lobe with the limbic system.
Psychiatry 1989; 52: 742±8.
2380 D. T. Stuss et al.

Stuss DT, Alexander MP, Palumbo CL, Buckle L, Sayer L, Pogue J. Walker MP, Ayre GA, Cummings JL, Wesnes K, McKeith IG,
Organizational strategies of patients with unilateral or bilateral O'Brien JT, et al. The Clinician Assessment of Fluctuation and the
frontal lobe injury in word list learning tasks. Neuropsychology One Day Fluctuation Assessment Scale. Two methods to assess
1994a; 8: 355±73. ¯uctuating confusion in dementia. Br J Psychiatry 2000; 177: 252±6.
Stuss DT, Pogue J, Buckle L, Bondar J. Characterization of stability Wei WW. Time series analysis. Redwood City (CA): Addison-
of performance in patients with traumatic brain injury: variability Wesley; 1990.
and consistency on reaction time tests. Neuropsychology 1994b; 8:
316±24. West R. Age differences in lapses of intention in the Stroop task. J
Gerontol B Psychol Sci Soc Sci 1999a; 54: 34±43.
Stuss DT, Shallice T, Alexander MP, Picton TW. A
multidisciplinary approach to anterior attentional functions. Ann West R. Visual distraction, working memory, and aging. Mem

Downloaded from https://academic.oup.com/brain/article-abstract/126/11/2363/403725 by guest on 26 March 2020


NY Acad Sci 1995; 769: 191±211. Cognit 1999b; 27: 1064±72.

Stuss DT, Alexander MP, Hamer L, Palumbo C, Dempster R, Binns West R, Murphy KJ, Armilio ML, Craik FIM, Stuss DT. Effects of
M, et al. The effects of focal anterior and posterior brain lesions on time of day on age differences in working memory. J Gerontol B
verbal ¯uency. J Int Neuropsychol Soc 1998; 4: 265±78. Psychol Sci Soc Sci 2002a; 57, 3±10.

Stuss DT, Murphy KJ, Binns MA. The frontal lobes and West R, Murphy KJ, Armillio ML, Craik FIM, Stuss DT. Lapses of
performance variability: evidence from reaction time. J Int intention and performance variability reveal age-related increases in
Neuropsychol Soc 1999; 5: 123. ¯uctuations of executive control. Brain Cogn 2002b; 49: 402±19.

Stuss DT, Levine B, Alexander MP, Hong J, Palumbo C, Hamer L, Whyte J, Polansky M, Fleming M, Coslett HB, Cavallucci C.
et al. Wisconsin Card Sorting Test performance in patients with Sustained arousal and attention after traumatic brain injury.
focal frontal and posterior brain damage: effects of lesion location Neuropsychologia 1995; 33: 797±813.
and test structure on separable cognitive processes.
Wiesendanger M, Wise SP. Current issues concerning the
Neuropsychologia 2000; 38: 388±402.
functional organization of motor cortical areas in nonhuman
Stuss DT, Floden D, Alexander MP, Levine B, Katz D. Stroop primates. Adv Neurol 1992; 57: 117±34.
performance in focal lesion patients: dissociation of processes and
Wilkins AJ, Shallice T, McCarthy R. Frontal lesions and sustained
frontal lobe lesion location. Neuropsychologia 2001; 39: 771±86.
attention. Neuropsychologia 1987; 25: 359±65.
Stuss DT, Alexander MP, Floden D, Binns MA, Levine B,
Woods DL, Knight RT. Electrophysiologic evidence of increased
McIntosh AR, et al. Fractionation and localization of distinct
distractibility after dorsolateral prefrontal lesions. Neurology 1986;
frontal lobe processes: Evidence from focal lesions in humans. In:
36: 212±16.
Stuss DT, Knight RT, editors. Principles of frontal lobe function.
Oxford: Oxford University Press; 2002a. p. 392±407. Zahn TP, Mirsky AF. Reaction time indicators of attention de®cits
Stuss DT, Binns MA, Murphy KJ, Alexander MP. Dissociations in closed head injury. J Clin Exp Neuropsychol 1999; 21: 352±67.
within the anterior attentional system: effects of task complexity Zahn TP, Kruesi MJP, Rapoport JL. Reaction time indices of
and irrelevant information on reaction time speed and accuracy. attention de®cits in boys with disruptive behavior disorders. J
Neuropsychology 2002b; 16: 500±13. Abnorm Child Psychol 1991; 19: 233±52.
van Zomeren AH, Brouwer WH. Clinical neuropsychology of Received August 15, 2002. Revised January 6, 2003.
attention. New York: Oxford University Press; 1994. Second revision May 16, 2003. Accepted May 19, 2003

You might also like