Brain Mechanisms

Neurobehavioral systems for attack and defense. Major recent developments in the study of animal aggression center around the realization that there are two distinct but complementary neurobehavioral systems functioning in aggressive encounters. These systems are polarized in the attack of a dominant or alpha rat on a strange intruder into the alpha's territory; in this case the two combatants show virtually no overlap in behavior; their actions have diametrically opposite effects; and the strength of the two patterns, alpha attack and defense, are differentially influenced by major independent variables such as pain, the presence of threat stimuli, or pharmacological and brain manipulations. The point is that there are a number of areas of evidence providing consistent and absolute (rather than statistical) differentiation of attack (which Adams calls offense) and defense (see Blanchard and Blanchard 1977).

Adams here proposes a further subdivision, creating categories of "defense" and "submission" from the original defense pattern. This distinction is clearly the major focus of the present treatment and constitutes one of our principal points of disagreement with Adams's review.

We do not believe there is a single area of evidence providing adequate grounds for a distinction between submission and defense "motivational systems". Adams cites a number of factors that he believes will differentiate the two, but not one of them is clear and consistent enough to serve as a criterion for the distinction. First, defense is described as characteristic of wild rats and rats with forebrain lesions, while submission is typical of the laboratory rat. In direct comparison of wild and laboratory Rattus norvegicus in conspecific encounters, we (Takahashi and Blanchard, submitted for publication) have found consistent similarities between the two strains for both attack and defensive behaviors, including those behaviors constituting Adams's defense and submission categories. Both strains show ultrasonic vocalization and lying on the back (which Adams characterizes as solely submissive behaviors, in contrast to a larger group of behaviors that can be either defensive or submissive). In fact, the wild rats show somewhat higher levels of lying on the back (the "full submissive posture") than do lab rats. Both strains also show occasional instances of retaliatory biting attack (defense) to a conspecific who has just bitten them. The only area in which there is a substantial difference between wild and lab rats is that the former are more reactive to such stimuli as human experimenters and will bite if cornered or handled. However, these same animals will preferentially run away from a human if escape is possible. At present the most parsimonious interpretation of differences between wild and lab rats is that the process of domestication involved self-selection (through differential breeding rates), and perhaps caretaker selection, for animals with reduced defensive attack and flight behaviors. As to rats with forebrain lesions, which Adams also characterizes as more defensive and less submissive, the "septal syndrome" animal actually shows increases in "submissive" behaviors such as ultrasound, freezing, and boxing, which are at least as profound as its increased defensive biting (Blanchard et al 1979).

Adams further suggests that the distinction between submission and defense lies in the primary purpose of the constituent behaviors. Defense serves to protect through the infliction of pain or other noncommunicative actions, while submission serves primarily as communication. This reflects the traditional interpretation that certain behaviors, notably lying on the back, have no intrinsic defensive function but actively inhibit the attack of a conspecific through the signal of defeat or submissiveness. We have argued elsewhere (Blanchard and Blanchard 1977) that these behaviors do serve a specific function in protecting the primary targets of conspecific biting attack, and that there is little reason to believe that such behaviors of a rat can serve as unconditioned inhibitors of the attack of a conspecific. These arguments, based on detailed analyses of attacker and defender interactions during conspecific fights (Blanchard et al 1977), are much too long to recapitulate here. However, it should be noted that Adams does not present evidence or analysis contrary to this view, In fact, he appears to agree with our suggestion that such actions as boxing and lying on the back serve to protect the specific sites bitten during conspecific fights. But at the same time, he uses the "primary signal function" of these acts as a major criterion to distinguish them from acts that are purely defensive. We think this simply doesn't work: to an experienced animal, any consistent defensive (or offensive) act may have a learned signal value or function, by virtue of its previous association with a specific outcome. For example, an attacking rat faced with the skilled defensive behavior of an experienced intruder may cease attack more quickly than when a naive intruder is used. The initial attack latency and actions are the same, but a skilled defense reduces or eliminates the possibility of a successful bite by the attacker, and the experienced attacker appears to recognize this. The "signal" function of most, if not all, defensive acts may be based on association with the protection afforded by the defensive value of the act rather than standing in opposition to such a defensive function. Ultrasonic vocalization may possibly be regarded as an exception to this statement, as it has no obvious primary defense function (except possibly as an alarm to conspecifics). However, the evidence that conspecific attack is actually inhibited by ultrasonic vocalization is indirect and unconvincing. Finally, Adams states that the present classification is based ultimately upon the neural circuitry involved, which we take to mean that major evidence for differences between submission and defense may be found in the extent to which brain manipulations differentially influence these behaviors. Since physiological studies of aggression and defense involve a heterogenous group of behavioral measures, there is necessarily much judgment and interpretation involved in attempting to evaluate effects on "submissive behavior" as opposed to "defense." We therefore examined four of Adams's citations listed in support of neural differentiation of these behaviors, in an effort to determine how compelling the evidence actually is.

Thus, Veening (1975) is described as having reported that "'if electrical stimulation is confined within the ventromedial hypothalamus, the effect is suppression of defense without fleeing." The actual Veening report is brief, the relevant portion (in its entirety) stating that "During stimulation not only feeding but also resting, sexual and aggressive behavior became clearly depressed in frequency and duration, whereas some other behavioral elements, such as sniffing and locomotion, showed increases..." There is absolutely no description of this aggressive behavior to indicate how Adams could decide that it constituted defense without fleeing, nor is there any indication that the locomotion increase reported had anything to do with flight.

Rodgers and Brown (1976) and Rodgers et al (1976) are both described by Adams as reporting that chemical stimulation of different amygdaloid nuclei "can increase boxing in response to footshock Without facilitating the lunge and bite response of defense." In fact, the sole response measure reported in each of these articles was the percentage of attack, which was defined as "lunging forward or... making a striking motion..." at the other animal. Boxing alone was measured separately, but the results were not reported. It was this "attack" measure that increased after stimulation, and that Adams has evidently interpreted as representing boxing without lunge and bite. I might add that we share Adams's implicit view that reflexive fighting depends on boxing, but if any bites or lunges at the opponent do occur, they are counted as fights; an increase in reflexive fighting certainly cannot be used as evidence that lunge and bite behaviors have not increased.

Finally, the results of Baxter (1967) are described as follows: "Whereas electrical stimulation in the hypothalamus of the cat produces defense carbachol from the same electrode produces submission when the chemical stimulation effect was blocked, the electrical stimulation effect remained intact..."

What is crucial here consists of two points made in the Baxter article but not mentioned by Adams. First, the carbachol effect was almost certainly not due to stimulation of the same site. It could be produced by stimulation of other structures, and especially after injection into the ventricular system, in which case the latency of the effect was less than for hypothalamic injection. So an implied claim of differentiation of defense and submission by stimulation of different elements at the same site is not viable.

Second, Baxter noted that, although his cats retreated from a gloved hand after carbachol stimulation, they "vigorously clawed and bit the experimenter" if picked up, attacking so strongly as to necessitate the use of a transfer cage in moving them. This Obviously is not in accord with the claim that carbachol enhances submission but not defensive attack.

These examples were not the result of checking a large number of sources, then selecting those that showed poor agreement with Adams's interpretations, They were the first and only ones checked, and they were selected solely on the basis that Adams used them as support for his contention that defense and submission follow separate but parallel pathways in the brain. They provide consistent documentation for the argument that cleaner response measures are needed for studies of the neural basis of attack and defensive behaviors (Blanchard and Blanchard 1977). More to the present point, however, they indicate how weak is the case for neural separation of submission and defense "motivational systems."

Leaving this area of disagreement aside, it should be said that Adams has shown tremendous grasp of a range of physiological and behavioral phenomena, making a brave attempt to analyze a literature as complex and confusing as it is important. Much of this confusion is due to behavioral problems which (we hope) are well on the way toward solution. Another source of impending clarification concerns the pharmacology of the systems for which anatomic aspects were primarily discussed here. In sum, we foresee, in the near future, sizeable strides in understanding the physiological bases of attack and defensive behaviors in animals, and their human analogues of angry aggression and fear. Adams's review contributes greatly to this progress by bringing together a scattered literature, and by serving as a source of hypotheses for future work.