Quay (92) speculates that ADHD, CD, and anxiety/withdrawal (AW) disorder can be differentiated in terms of Gray's (124) theory of two important control systems: a behavioral inhibition system (BIS) and a behavioral reward system (REW). In Gray's theory, increases in responding brought about by positive reinforcement ("hope") and by both active avoidance and escape paradigms (reward is escape from punishment, or "relief") are under the control of REW. Reductions in responding that occur in extinction procedures and passive avoidance are under the control of BIS. Anxiety is activity in the BIS that is cued by conditioned stimuli that signal fear or frustration. Predatory aggression, on the other hand, is under the control of REW. Gray has postulated anatomic loci for these two systems: the reward system corresponds to the catecholaminergic structures mediating the rewarding effects of self-stimulation of the brain (228). The BIS, a supposed noradrenergic system, is localized in the lateral and medial septal areas and in the connections of these to the hippocampus.
Stimulant drugs enhance the activity of both REW and BIS. Quay speculates that there is a relatively greater enhancement of BIS than of REW in ADHD children given stimulant medication, thus bringing the two systems into balance. He concludes that ADHD children have a deficiency in the BIS system, noting that antianxiety medications tend to affect them adversely. Again and again, deficiencies in inhibition are emphasized, beginning with the early papers of Luria (7). Because amphetamine improves passive avoidance but does not improve CD, and because catecholamine antagonists (haloperidol and propranolol) appear to decrease CD, Quay suggests that CD seems most related to oversensitivity to reward. He attributes anxiety/withdrawal disorders to an overactive BIS. Gray's two systems are supported by a considerable amount of experimental evidence and the extrapolations of Quay appear to be very reasonable. In particular, autonomic studies of heart rate and skin conductance reactivity suggest that HY children are more difficult to arouse than normal children, which supports Quay's notion of an underactive BIS.
9.2. Barkley's Theory of Response Inhibition
Judging by recent reports on ADHD children it appears that Barkley's theory is slowly but surely becoming the preferred theory for most writers. He is concerned only with the HY-impulsive type and mainly with the explanation of IMP. Barkley (22) defines response or behavioral inhibition as consisting of three interrelated components:
1. Inhibiting the initial prepotent response to an event.
2. Stopping an ongoing response or response pattern, thereby permitting a delay in the decision to respond or continue responding.
3. Protecting this period of delay and the self-directed responses that occur within in it from disruption by competing responses (interference control).
Barkley ties self-regulation to response inhibition and interference control, saying that "there can be no actions taken toward the self aimed at modifying a future consequence related to an event if the individual has already responded to that event." This appears to mean that any opportunities to modify an outcome must occur in the period of inhibition (delay) of the prepotent response, including the timing of when it is to be executed. Inhibition protects the self-directed and often covert actions to the self that occur in the delay period, protects the prepotent responses that are about to be executed, and protects against extraneous sources on interference.
According to Barkley, executive function (EF) and self-regulation depend on response inhibition, and the problems of ADHD children, particularly their impulsiveness, result in deficiencies in EF and the psychosocial processes they control, e.g., time estimation and inner speech. In an article in which Barkley (229) responds to criticism of his theory, he says, "Nevertheless, unlike other views of EF and ADHD, the model I have set forth though certainly imperfect, is far more specific about the origins and nature of EF and more closely aligned with an evolutionary perspective than any view yet proposed of either of these domains." He claims that the deficits in EF are devastating and that they are far more important in understanding the problems of ADHD children than their trivial impairment in capacity to pay attention. I would not disagree with the impairment in EF as being important, but would only add that perhaps the most important EF is the capacity to focus attention and ignore distracting thoughts and stimuli. It is also obvious that there are many different EFs and control mechanisms involving relations of frontal lobes with other structures in the brain, and even variations in control of different types of attention (sustained, selective). So it is somewhat of a misnomer to speak as though there is only one EF. Barkley, however, is apparently talking about only those EF functions that are affected by or related to ADHD, but it is difficult to know where these leave off and others begin.
9.3. Pavlov's Ignored Contributions
Many of these concepts discussed above have a counterpart in the writings of Pavlov (18,19) in providing insights into the nature of inhibition that are not generally known. A prepotent response for Barkley is a conditional response (CR) for Pavlov, and it can be negative (inhibitory) or positive (excitatory). This definition could be expanded a bit to include any kind of instrumental learning, including operant responses. Most psychologists have finally discovered that you cannot teach a rabbit to swim like a duck (230). So all learning depends on some inherent biological structure, whether a fear of snakes or the learning of a language. In simple differential conditioning there are two stimuli, one that is reinforced (more accurately paired in the case of Pavlovian conditioning) and one that is not reinforced (231). The negative conditional stimulus (CS) never reinforced produces responses of some kind (no zero level attained) in the conditioning of heart rate, blood pressure, or urinary retention. However, more precise and less generalized systems, such as salivation in anticipation of food and motor actions to avoid noxious stimuli, do attain a no-appearance (zero) level with repeated nonreinforcements. However, in neither case does the level of response measure the depth of inhibition. Pavlov showed in a variety of experiments that the inhibitory state deepens with additional pairings and this does not show up in the negative CR being partial or completely absent. The number of trials it takes to convert a negative CS to a positive CS increases as a function of the number of presentations of the negative CS.
Pavlov also showed that the elaboration of a trace CR (CS terminates before unconditioned stimulus [US] onset) or delayed CR (US overlaps the CS but there is a delay of 5-60 s or more between the onset of CS and US) is associated with a period of inhibition known as the "inhibition of delay". The period of inhibition, which can be interrupted by distracting stimuli (disinhibition) but less so the better established the response (the greater the number of reinforcements). This would seem to be akin to the protective delay of Barkley. Pavlov was insistent that inhibition of the type described here was mediated by the cortex; he referred to it as internal inhibition, in contrast to the type of direct inhibition seen in antagonistic muscular responses or reflexes. I would argue that dogs must also be capable of self-regulation to some extent if they can refrain from making premature responses and resist the onslaughts of distracting stimuli. However, Pavlov recognized an excitable type of dog, not unlike ADHD children in temperament, that had great difficulty in developing delayed or trace CRs. In one series of very interesting experiments, Pavlov's group found that if a delay interval—say, of 15-20 s— is firmly established, it is very difficult and some instances impossible to change to a shorter interval. Even if the CS-US interval is shortened, the CR may continue to occur at the previously established delay interval.
These early findings seem to us to support many of the conjectures of Barkley, including those mentioned by the prominent writers he references (232-234). Pavlov and his associates studied individual animals intensively over long periods of time. His null or no hypothesis was not a statistic but an experimental manipulation to prove a point. It is a shame that the books that do mention his work do so in such a cavalier and superficial manner.
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