Sergeant 2000
Sergeant 2000
BIOBEHAVIORAL
REVIEWS
Abstract
Attention Deficit/Hyperactivity Disorder (ADHD) is a childhood psychiatric disorder which when carefully defined, affects around 1% of
the childhood population [Swanson JM, Sergeant JA, Taylor E, Sonuga-Barke EJS, Jensen PS, Canwell DP. Attention-deficit hyperactivity
disorder and hyperkinetic disorder. Lancet 1998;351:429–433]. The primary symptoms: distractibility, impulsivity and overactivity vary in
degree and association in such children, which led DSM IV to propose three subgroups. Only one of these subgroups, the combined subtype:
deficits in all three areas, meets the ICD-10 criteria. Since the other two subtypes are used extensively in North America (but not in Europe),
widely different results between centres are to be expected and have been reported. Central to the ADHD syndrome is the idea of an attention
deficit. In order to investigate attention, it is necessary to define what one means by this term and to operationalize it in such a manner that
others can test and replicate findings. We have advocated the use of a cognitive-energetic model [Sanders, AF. Towards a model of stress and
performance. Acta Psychologica 1983;53: 61–97]. The cognitive-energetic model of ADHD approaches the ADHD deficiency at three
distinct levels. First, a lower set of cognitive processes: encoding, central processing and response organisation is postulated. Study of these
processes has indicated that there are no deficits of processing at encoding or central processing but are present in motor organisation
[Sergeant JA, van der Meere JJ. Convergence of approaches in localizing the hyperactivity deficit. In Lahey BB, Kazdin AE, editors.
Advancements in clinical child psychology, vol. 13. New York: Plenum press, 1990. p. 207–45; Sergeant, JA, van der Meere JJ. Additive
factor methodology applied to psychopathology with special reference to hyperactivity. Acta Psychologica 1990;74:277–295]. A second
level of the cognitive-energetic model consists of the energetic pools: arousal, activation and effort. At this level, the primary deficits of
ADHD are associated with the activation pool and (to some extent) effort. The third level of the model contains a management or executive
function system. Barkley [Barkley RA, Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of
ADHD. Psychological Bulletin 1997;121:65–94] reviewed the literature and concluded that executive function deficiencies were primarily
due to a failure of inhibition. Oosterlaan, Logan and Sergeant [Oosterlaan J, Logan GD, Sergeant JA. Response inhibition in ADHD, CD,
comorbid ADHD 1 CD, anxious and normal children: a meta-analysis of studies with the stop task. Journal of Child Psychology and
Psychiatry 1998;39:411–426] demonstrated that this explanation was not specific to ADHD but also applied to children with the associated
disorders of oppositional defiant and conduct disorder. Other executive functions seem to be intact, while others, are deficient. It is argued
here that the cognitive-energetic model is a useful guide for determining not only ADHD deficiencies and associated disorders but also
linking human cognitive neuroscience studies with neurobiological models of ADHD using animals [Sadile AG. Multiple evidence of a
segmental defect in the anterior forebrain of an animal model of hyperactivity and attention deficits. Neuroscience and Biobehavioral
Reviews, in press; Sagvolden T, Sergeant JA. Attention-deficit hyperactivity disorder: from brain dysyfunctions to behaviour. Behavioural
Brain Research 1998;94:1–10]. A plea for an integrated attack on this research problem is made and the suggestion that conceptual
refinement between levels of analysis is essential for further fundamental work to succeed is offered here. q 2000 Elsevier Science Ltd.
All rights reserved.
Keywords: Cognitive-energetic model; Attention deficit hyperactivity disorder; Psychiatric disorder; Executive functioning; Attention; Inhibition
administered to both ADHD and control children, ADHD reflecting a difference in energetic condition between
children increased in striatal activation. ADD and controls rather than a strict failure of inhibition.
A recent fMRI study has shown that during the stop-task,
ADHD adolescents had hypofronatlity, specifically, at the
2.3. Stop-signal task right caudate and right mesial frontal [35]. Correlations
between response execution and the basal ganglia (left
The stop-signal task is currently the most direct measure globus pallidus and caudate symmetry) significantly
of the processes required in inhibiting a response [18]. In differed between ADHD boys and controls [6]. When
this task, subjects are instructed to respond when a signal is controlled processing (fast but accurate responding is
presented and to inhibit their intended response to the signal required) has been used, size of the right anterior cingulate
when a stop-signal (usually a tone) is presented. Stop signals gyrus is correlated in normal children with speed and accu-
are presented at different intervals before the subject’s racy of performance [7]. It would be of interest for fMRI
expected response. The closer the stop signal is presented studies to determine this relationship in ADHD children,
to the “point of no return”, the more difficult it becomes to since both speed and accuracy of responding in ADHD
inhibit the response. This task, in contrast to the go/no-go children is disturbed [42,43]. Further, the basal ganglia
paradigm, requires suppression of a response, which is has been shown to be crucial in mediating the connection
already in the process of being executed. Even when stop between the executive functions assumed under the
signals are internally related, i.e. presented at fixed intervals management system and attention processes associated
dependent upon stimulus presentation, as opposed to being with the thalamus [16,28]. Caution is needed in attributing
presented at fixed intervals dependent upon the go response, significance to a particular cortical structure, since it has
ADHD children can be successfully distinguished from been recently demonstrated that the posterior inferior
controls [34]. lobules (VIII–X) of the cerebellum are significantly reduced
Recently, a meta-analysis of eight studies employing the in ADHD boys [3].
stop-signal task studies was conducted [22]. For the first
dependent variable, the inhibition function, consistent and 2.4. The change task
robust differences were found between ADHD and control
In order to study the EF, controlled adaptive functioning,
children; ADHD children were less able to inhibit inap-
the ability to suppress a response and subsequently initiate
propriate responses than controls.
an alternative response (response re-engagement) has been
ADHD children also had slower SSRTs than controls.
used in an extension of the stop-signal task; the change task.
Thus, poor response inhibition was attributed to slow inhi-
Results of studies using this task [38,39,23] confirm earlier
bitory processing. For the third dependent variable, ZRFT-
reports using the stop-signal task that ADHD children are
slope, no group differences were found; ADHD children did
less able to inhibit a response compared to controls. Further,
not differ from controls in their ability to trigger an inhibi-
these studies replicated the finding of slower inhibitory
tory response or in variability in the latency of the inhibitory
processing in ADHD children than controls. ADHD chil-
process. However, Conduct Disordered (CD) children
dren were also observed in two of these studies [38,39] to
showed similar impairments to ADHD children. Therefore,
have slower response re-engagement than controls. Despite
the meta-analytic findings do not support the notion that
being able to demonstrate a slower SSRT in the ADHD, no
response inhibition deficits are specifically related to
difference in change reaction time was found between
ADHD. Rather, the results suggest that poor response inhi-
ADHD and controls [23]. This suggests that the speed of
bition characterises children with behaviour characterised as
this EF is intact in ADHD children.
disruptive.
In summary, the stop-signal studies indicate that ADHD
The stop-signal task contains a third measure, ZRFT,
children are less likely to inhibit a response than controls.
which is the probability of triggering or inhibitory process.
However, measures of inhibition do not differentiate ADHD
In their meta analysis [22] no difference was found for this
children from CD children so that the stop-signal findings
measure between ADHD children and controls nor between
are not specific with respect to ADHD. This finding is
ADHD and CD subjects or CD and control children. ZRFT
consonant with the report that EF tests are significantly
is unable to explain the observed lack of inhibition to the
correlated with the degree of aggression observed in teenage
stop-signal.
boys [40].
The stop-task has been used with ADD children and
simultaneously their EEG recorded and analysed with low 2.5. Inhibitory effect of error detection
resolution electromagnetic tomography [4]. This study
reported that failures to inhibit in a stop task by ADD chil- As noted earlier, the cognitive-energetic model was
dren was related to an early brain potential N1, which designed to include a superordinate, management or evalua-
appeared posteriorly too early to be evoked by the stop- tion mechanism. Vigilance researchers had shown that
signal. This suggests that the actual brain-state of the knowledge of results enabled the subject to adjust so as to
ADD child does not meet the required state and may be improve performance. It has been demonstrated [33] that
10 J. Sergeant / Neuroscience and Biobehavioral Reviews 24 (2000) 7–12
subjects can correct errors faster than they can make correct terms such as motivation and response to contingencies,
responses. Presumably, this means that the subject detects which are also thought to be disrupted in ADHD children.
the error and error correction is actually initiated before Recent fMRI research has suggested that attentional activity
completion of the incorrect response. However, on the recorded in the ventral thalamus is seen under low activation
trial following an error, the subject takes more time to but when caffeine is administered (and activation
respond, apparently, to ensure that a correct response is increased), thalamic activity is substantially increased [28].
made. This is known as RT after an error RTE 1 1; the A brief review of studies from an energetic model are
“1” indicating first correct trial after an error. Active control presented below.
of processing of allocation of attentional resources on
RTE 1 1 trials requires inhibition of responding. 3.1. Event rate and response inhibition
It was noted from Ref. [11] that both the supplementary
Event rate, the speed with which stimuli are presented,
motor area and the anterior cingulate were shown in tasks to
was shown to be an important determinant of performance
be involved in error detection and compensation [12]. Given
and to have its locus in the activation pool [36]. Event rate
the highly focused nature of the effect at FzS, it would seem
alters the energetic state of the subject, i.e. compared with
that source of the generator may be relatively superficial and
the medium condition, the fast condition may induce either
close to the scalp [11].
over arousal or over activation, resulting in fast-inaccurate
It has been shown that as cognitive load increased in a
responding. A slow event rate may induce under arousal or
search task, controls slowed RTE 1 1 in a linear fashion
under activation, resulting in slow inaccurate responding
[41]. ADHD children did not perform in this manner.
[36]. Vigilance measures such as the Continuous Perfor-
When the processing load was low, ADHD children had a
mance Task (CPT) have been used to track loss of energetic
much slower RTE 1 1 than controls. In contrast, when the
allocation of periods of time [26]. Recently, in a group of
processing load was high and one would expect a slow
both children and adult ADHD subjects, fMRI has shown
RTE 1 1; ADHD children were faster than controls.
that in a CPT the predominant activity in this task was
Recently, RTE 1 1 has been shown to become slowed by
located at the right middle frontal gyrus [49]. However,
MPH [15]. Drugs are considered as influencing both ener-
differentiation of attention and activation effects was not
getic and computational factors in the cognitive-energetic
made in this study [28].
model. The finding of Krusch et al. indicates the influence of
Event rate differentiates controls from ADHD children in
an energetic factor on executive processing.
a wide variety of tasks [8–10,20]. In general, ADHD chil-
Since both overly slow and overly fast RTE 1 1 latencies
dren have been found to perform more poorly in conditions
were observed in ADHD children, and since poor inhibition
of relatively slow event rates as compared with fast and
would have predicted only fast RTE 1 1; it would seem that
moderate event rates.
these findings argue against a disinhibition hypothesis. A
ADHD children with and without a Tic Disorder (TD)
failure to adjust to task demands, referred to as attentional
were compared with a normal control group, using a go/
allocation [46], would seem to offer a better account of these
no-go task [19]. Stimuli were presented at three rates: a
findings.
fast presentation rate (1 s), a medium presentation rate
In summary, three tasks: the “go/no-go”, stop-signal and
(4 s) and a slow presentation rate (8 s). Results indicated
change task provide support for the inhibition hypothesis.
that ADHD children with and without comorbid TD made
The stop-signal and change tasks indicate that a slow inhi-
more errors of commission (i.e. responses to the No-Go
bitory process underlies poor response inhibition in ADHD
stimuli) than controls. Of interest was the finding that the
children, but this is not specific to this group: inhibitory
inefficient task behaviour of ADHD-only children was
performance measures do not differentiate ADHD from
related to the event rate. ADHD children made more errors
CD children. Few reports are available to determine whether
of commission in the fast and slow conditions, but not in the
claims of an inhibition deficit are specific only to ADHD or
medium condition, thus substantially replicating the find-
other externalizing disorders.
ings of Ref. [20]. These results suggest that ADHD chil-
dren’s lack of response inhibition is modulated by their
inability to adjust their state.
3. Energetics
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