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Attention-deficit/hyperactivity disorder
(ADHD) is a developmental disorder with the cardinal features of difficulties
with sustained attention, distractibility, hyperactivity, and impulse
control. It arises early in childhood, typically between 3 and 7 years
of age. The disorder is relatively stable over time and persists through
adolescence and into adulthood in more than half the cases. A significant
proportion of children will experience school failure and will develop
conduct disorders, delinquent activities, and antisocial personalities.
As a result, the burden of ADHD to affected individuals, to their families,
and to society is considerable.
Over the next several months, this
column will explore the underlying mechanisms that contribute to the disorder.
The first columns will review the concept of executive functioning and
the role the frontal cortex has in regulating mental skills that are required
to sustain attention and inhibit impulsive behavior. Particular attention
will be given to neurotransmitter systems that are thought to play a critical
role in frontal cortical activity. The next 2 columns will be devoted
to recent progress in the genetics of ADHD. Finally, we will review whether
animal models of hyperactivity have been useful in furthering our understanding
of the underlying etiology of the disorder. It is important to note at
the outset that ADHD is not a unitary illness. It is likely that a number
of different pathways that include both genetic and environmental factors
contribute to the expression of its symptoms.
The most prevalent clinical view of
ADHD maintains that the central deficits of the disorder are the inability
to sustain attention and symptoms of hyperactivity and impulsivity. However,
this view of ADHD is only a description of the most commonly observed
characteristics. It is not a theory that could serve as a useful scientific
tool for researchers, nor does it point us to the underlying neural pathways
that might be involved.
Over the past 2 decades, tremendous
progress has been made in understanding the functions of the prefrontal
cortex (Fig.
1). This progress has led to an
appreciation of how this region of the brain regulates specific mental
activities that allow for self-control. These mental activities are unified
under the term executive functions. This initial column will review
recent theories of executive functioning and will review how deficits
in executive functions occur with deficits in the development, structure,
and function of the frontal cortex and its networks with other brain regions,
such as the basal ganglia.
Karl Pribram may have been the first
to describe the executive role of the prefrontal cortex when he concluded
that it is "critically involved in implementing executive programs
where these are necessary to maintain brain organization in the face of
insufficient redundancy in input processing and in the outcomes of behavior"
(Pribram, 1976, p. 509). Muriel Lezak defined executive function (EF)
as "those capacities that enable a person to engage successfully
in independent, purposive, self-serving behavior" (Lezak, 1995, p.
42). Actions are executive if they involve the "when" or "whether"
aspects of behavior, whereas nonexecutive functions involve the "what"
and "how." Left unclear in the vast neuropsychological literature
on EF is any operational definition of what is encompassed by the term
executive. The term executive functions seems to incorporate:
• Volition, planning, and purposive,
goal-directed, or intentional action.
• Inhibition
and resistance to distraction.
• Problem-solving and strategy
development, selection, and monitoring.
• Flexible shifting of actions
to meet task demands.
• Maintenance of persistence
toward attaining a goal.
• Self-awareness across
time.
Many authors have recognized the substantial
overlap or interchangeability between EF and self-regulation. Maureen
Dennis saw EF as partly social in nature (discourse and reciprocity).
Stuart Dimond defined EF as entirely involving social intelligence (management
of day-to-day social conduct). Others have simply lamented the lack of
definition and declared EF to be what the frontal lobes do.
A leading candidate for one EF is
working memory (WM). This is the capacity to hold a mental representation
in mind to guide behavior. It is remembering in order to do. Often, the
remembering must span a period of time so long that the remembered external
events may no longer exist. The performance of the act must be linked
to the arrival of some mentally conjectured future event. Time, timing,
and timeliness in behavior are regulated in part by this EF, as Juaquim
Fuster noted. Others, like Baddeley, suggested that WM had 3 components:
(1) a visual-spatial sketchpad (nonverbal working memory), (2) verbal
working memory and its associated phonological loop (private self-speech),
and (3) a central executive. The central executive (3) enslaves (1) and
(2) for its purposes (the overall goal to be achieved). Little is said
about the nature of this central executive.
Another candidate EF is response inhibition.
It is critical to WM in providing the initial delay in the response to
an event during which WM is often activated; the protection to WM from
interference by unrelated yet competing external and internal events;
and the interruption of ongoing response patterns being guided by WM should
they prove ineffective in attaining the goal.
A Theoretical Model of Executive Function
The history of the model below and
its supporting research appear in my earlier textbook, ADHD and the
Nature of Self-Control. It is drawn from the work of Jacob Bronowski,
Juaquim Fuster, Patricia Goldman-Rakic, and Antonio Damasio. Its components
appear in Table 1 along with those psychological and social abilities
hypothesized to result from each EF.
Each EF contributes to the following
developmental shifts in the control over human behavior:
• From external events to mental
representations related to those events.
• From
control by others to control by the self.
• From immediate reinforcement
to delayed gratification.
• From the now to the conjectured
social future.
Each EF probably arises by a common
process:
• It originates in a general class
of observable behavior toward others as a means of predicting and controlling
the outside world.
• This
class of behavior is then turned on the self as a means of controlling
one’s own behavior, yet such behavior may remain publicly observable
for a period of development before becoming covert.
• It then becomes progressively
private or covert (internalized) in form; that is, its associated musculoskeletal
movements are suppressed while its execution within the brain continues.
Self-regulation (SR) can be defined
as any self-directed action that serves to alter the probability of a
subsequent response so as to alter the likelihood of a future consequence.
Each EF is a type of self-directed action. Consequently, SR is an inherent
part of EF, making EF inherently future-directed. The EFs are response
inhibition and those 4 general classes of self-directed actions humans
use to engage in SR toward conjectured social futures:
• Self-directed sensing (sensory-motor
action) that creates nonverbal WM.
• Self-speech
that creates verbal WM.
• Emotion/motivation to
the self that creates intrinsic goal-directed motivation.
• Self-directed play that
creates inventiveness, fluency, and flexibility in goal-directed behavior.
The developmental progression common
to each EF is typified in the internalization of language. As the child
matures, speech toward others becomes speech to the self yet, for a time,
vocalized. It then progresses to subvocal self-speech and finally to fully
covert or private speech that comprises verbal thought. The EFs act in
concert to achieve the overarching goal of a net maximization of long-term
social (economic) rather than more immediate outcomes for the individual.
Thus, as Dimond, Vygotsky, and Luria all argued, the adaptive problems
that the EF/SR system evolved to solve must be social in nature, making
the EF/SR system the seat of social intelligence.
Response inhibition is the capacity
to delay a response to an immediate environmental event. Delayed responding
provides the foundation on which EF/SR develops. SR is impossible without
a delay in that response directed toward immediate reinforcement. Response
inhibition also permits the "internalization" or "privatization"
of each EF. It does so by suppressing the observable musculoskeletal movements
associated with the self-directed behavior that makes up each EF. Over
the course of development, this makes that behavior become covert or "mental"
in form. This is done so that the actions occurring during an EF cannot
be directly observed by others. That privatization is likely necessitated
by the selection pressures set up in a group-living species of self-interested
imitators whose closest evolutionary competitors are their peers.
I. Nonverbal Working Memory.
The first EF is nonverbal WM. Among the various senses, the most important
to humans are vision and, to a lesser degree, hearing. It is not surprising,
then, that this mental module is largely composed of visual imagery and
private audition. Undoubtedly the other senses also contribute to this
symphony of internalized resensing. It consists of 2 interrelated processes:
(1) the retrospective function, which is resensing the past information
and holding it online (in mind), making it largely a sensory activity;
and (2) the preparation of motor action initiated by the resensing of
the past, known as the prospective function. Together they provide
for the progressive development of a cognitive window on oneself across
time, or autonoetic awareness, and the subjective sense of time
more generally. The past and future tenses in human languages likely derive
their reference points from this WM. This EF grants humans the capacities
for generalized imitation and vicarious learning, self-awareness, social
exchange (delayed reciprocal altruism), and the more general capacity
for the cross-temporal organization of behavior. The evolution of this
EF likely permitted humans the capacity to engage in not only self-interested
cooperation and coalition formation but also the "theft" of
each other’s behavior (vicarious learning) rather than acquiring
it through the arduous process of trial-and-error learning. This would
have set up a selection pressure that required that self-directed actions
be made private so that one’s peers could not appropriate the behavior
prior to its more timely, opportunistic display. Given that mental representations
are icons, this EF may have created the initial step needed toward the
evolution of symbolization, from mental icons to indices, and then on
to symbols.
II. Verbal Working Memory.
This EF comprises the internalization of speech, as described above. It
is covert (silent) receptive and expressive language. Individuals are
afforded the same means of control over themselves that language serves
in the control of others, such as self-description, reflection, instruction,
and questioning. Rule discovery and rule-governed behavior more generally
(the motor-controlling functions of language) arise here. And so, eventually,
might hierarchically organized sets of rules about rules, or meta-rules
(meta-cognition). In conjunction with nonverbal WM, this EF permits both
reading comprehension and the moral guidance of behavior by internalized
rules.
III. Internalized Emotion/Motivation.
This function may well arise, at least initially, as a consequence of
the first 2 EFs. By re-presenting visual and verbal mental stimuli to
oneself, emotional and motivation states ensue. These states are Damasio’s
somatic markers. Initially, they may be observable to others, as when
a child laughs publicly in response to a privately reexperienced humorous
event. Eventually these affective states become covert. Emotions are motivational
states composed of level of arousal imposed on a reward/punishment gradient.
Thus, this EF creates the SR of private motivational states in the service
of future goals. It is the source of intrinsic motivation essential to
driving future-directed behavior.
IV. Reconstitution. This EF
likely arises from play. It consists of 2 interacting processes: analysis
(taking apart) and synthesis (recombining). These are applied to
the contents of the 2 WMs, thereby permitting the manipulation and dismemberment
of old experiences to synthesize novel responses. It is a form of ideational
darwinism in which the units of old experiences are recombined into novel
behavior that is judged against the goal to be attained so as to select
the most viable option. By so doing, as Karl Popper once noted, humans
allow their erroneous ideas to die in their place. Here originates the
flexibility, fluency, and inventiveness of human goal-directed actions.
In combination, the EFs provide a
powerful set of tools for SR toward the social future that is unparalleled
in any other species. The fields of science, art, and music, among others,
are likely examples of this set of skills.
Research overwhelmingly demonstrates
a deficit in response inhibition in persons with ADHD. Consequently, the
EF model predicts that secondary deficits (e.g., greater errors and variability
in performance) will arise in all other EFs. Deficits would then be detected
in the psychosocial abilities of each (Table
1). These important predictions
are an opportunity to test the model because those predictions are not
drawn from the literature on ADHD but from the literature on EF. Consistent
with these predictions, research on ADHD has found deficits in each EF.
However, the support varies across the functions, largely due to the limited
amount of research on some of them and the fact that much of that research
did not set out to intentionally test this model.
This theory shows that ADHD impairs
social intelligence through the cascading of deficits it creates throughout
the EF/SR system. Delays occur in the 4 developmental shifts in the control
of behavior. The attention deficits ascribed to ADHD can now be seen as
intention deficits (attention toward the future). This would cause
deficiencies in reciprocal altruism and vicarious learning in ADHD, among
other deficits in universal social activities requiring EF (e.g., coalition
formation, self-innovation, and social self-defense).
Suffice to say that there is much
here in need of future research to establish its veracity. But as the
time-limited tool that is any credible theory, its scientific and heuristic
value for understanding EF and its evolution as well as ADHD should be
evident.
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