Fig. 3.3. The Papez circuit has been proposed as a primary pathway for the expression and experience of emotion.
these theta waves, which are believed to be associated with the normal inhibitory functioning of the septohippocampal system (SHS). Theta rhythms are generated by the hippocampus in an area called the dentate gyrus but are under the control of pacemaker cells in the medial septum (Gray, 1982).
In line with such a processing-modulatory function is Gray's speculation that the hippocampus, together with other limbic areas interacting with the SHS, serves to excite or inhibit behavior selectively (Gray, 1982). In conjunction with the ARAS, for example, the SHS appears to detect novelty in the environment and mediates the expression of surprise or startle. The SHS also mediates other forms of adaptation, including the most primitive form of stimulus learning—habituation. Orienting response studies performed by Sokolov and Vinogradova (reported in Gray, 1971) have shown that novelty and habituation are processed by a comparator mechanism located in the SHS. This mechanism compares ongoing stimulation with an animal's expectations of what should be occurring. If the results of this comparison between what is expected and what actually occurs are different, the effect produced is novelty (surprise/startle) and the evocation of an appropriate orienting response or intensified vigilance. If the stimulation is identical to what the animal expects, then habituation will occur—the dog gradually takes no notice of it. Habituation is highly specific, however. Sokolov's studies have shown that subtle changes of the stimulus complex (e.g., intensity, duration, quality, repetitive rate, and association with other stimulus events) may trigger a comparator "alarm" with a resultant recovery of the habituated orienting response. This subtle type of sensory sorting has led Gray to speculate that novelty reaches the SHS by a thalamocortical route rather than through the ARAS, which appears to be more dedicated to attentional functions arising from painful stimulation. An immediate outcome produced by novelty is the inhibition of ongoing behavior—a kind of "stop and think" hesitation occurs whenever a dog is faced with something significant and new. When the comparator finds a significant difference between what is expected and what actually happens, it signals and ac tivates the behavior inhibition system (BIS). The BIS inputs cause ongoing behavior to stop. The BIS is particularly associated with punishment or frustrative nonreward. Both punishment and frustration disrupt ongoing behavior and subsequently invigorate or potentiate instrumental responding.
Another general system outlined by Gray involves the display of unconditioned escape behavior and affective aggression in response to fear- or anger-evoking stimuli. The flight-fight system (FFS) is predominately under the regulation and control of the hypothalamus and the amygdala. As previously discussed, the hypothalamus controls both affective aggressive displays and quiet predatory attacks.
Finally, Gray has postulated a behavioral activation system (BAS) operating in dopaminergic reward centers (nucleus accumbens) associated with the basal ganglia, neo-cortical structures, and various regulatory activities provided by the SHS, including important comparator functions. The BAS is associated with both the acquisition of reward and the termination or avoidance of punishment. The determination of whether a particular response is followed by reward or punishment depends on a comparator function. Voluntary behavior is self-reflective, requiring that at each moment the SHS evaluates the convergence or divergence of expected outcomes with what actually occurs. These various functions are coordinated by the pre-frontal cortex, resulting in organized learning based on positive-feedback loops involving a series of predictions and confirmations that culminate in general expectancies about behavioral outcomes. Three basic outcomes on voluntary behavior are possible as the result of such expectancies: acquisition, extinction, or maintenance. Behavior that is followed by positive consequences exceeding expected outcomes is strongly reinforced, whereas behavior attended by consequences that are overpredicted (receiving a reward smaller than expected) results in a weakening of the associated behavior. Finally, responses followed by outcomes that are well predicted lead to confirmation of previously established expectancies but result in no new learning.
The BAS and positive learning evolved to maximize direct contact with rewarding events and to avoid their loss or omission. in contrast, the BIS is concerned with the recognition of signals anticipating punishment, nonreward, or startle/novelty. In the presence of such signals, the BIS prompts an animal to inhibit ongoing behavior and to become more vigilant. The FFS involves affective displays aimed at removing fear-eliciting or threat signals by flight or attack. Gray (1991) postulated a theory of temperament that involves a combined contribution of these three systems. The BIS encodes relevant pathways and individual difference in the area of anxiety and impulsivity with heightened sensitivity to learning involving punishment; the FFS encodes traits predisposing an individual to various degrees of aggressive and defensive behavior, and the BAS is relevant to an animal's willingness to learn or alter behavior for positive reinforcement.
According to Rogeness (1994), conduct disorder in children may be conceptualized within the general framework of Gray's model. A child who is predominately controlled by reward mechanisms belonging to the BAS may be unable to adequately control maladaptive impulses that lead to immediate satisfaction. Such individuals are unable to inhibit consummatory behavior when faced with the immediate prospects of reward acquisition or escape-avoidance opportunities. Also, children with an underactive BIS may not condition well to signals predicting loss of reward or other forms of punishment. Since the BAS is mediated by dopaminergic activity and the BIS governed by noradrener-gic activity, one would expect in an impulse-biased child or dog greater dopamine activity and tone, as well as reduced noradrenergic function. An additional factor, especially relevant with regard to the expression of aggressive behavior in such cases, is serotonergic projections from the dorsal raphe bodies terminating in the amygdala—an important area for the inhibition of aggressive behavior. Serotonin plays an important role in the regulation and inhibition of aggressive behavior—decreased serotonergic activity in these systems is associated with an increased likelihood of aggressive impulsivity under conditions of threat or frustration.
A dog governed by a strong BAS (strong dopaminergic activity) tends to be one that gets into perpetual trouble, moving from one "jam" to another. Such dogs are swept up by the moment's opportunities and governed by the acquisition of immediate gratification and the calculation of escape-avoidance strategies with which to avoid punishment—all rewarding events. BIS (strong noradrenergic ac-tivity)-controlled dogs, on the other hand, are more circumspect and responsive to punitive events impinging on them; such dogs are more likely to inhibit their behavior in the future following punishment instead of perpetually making the same mistakes. Theoretically, dogs governed by strong BAS activity and regulated by a weak BIS together with reduced serotonergic modulation over amyg-daloidal interconnections are more likely to behave impulsively, possibly with episodic aggression. Perhaps, a diagnostic test differentiated by two biochemical parameters would be useful for the evaluation of certain forms of aggression: (1) evidence of decreased noradrenergic/serotonergic activity and (2) evidence of increased dopaminergic activity. Clinical investigations of drugs that inhibit the reuptake of NE and serotonin (e.g., amitriptyline and clomipramine) in conjunction with appropriately selective dopamine antagonists might prove very useful for the management of canine impulsive behavior disorders, including some forms of hyperac-tivity and aggression.
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