D.J. Albert

Aggression in humans: what is its biological foundation?

Although human aggression is frequently inferred to parallel aggression based on testosterone in nonprimate mammals, there is little concrete support for this position. High- and low-aggression individuals do not consistently differ in serum testosterone. Aggression does not change at puberty when testosterone levels increase. Aggression does not increase in hypogonadal males (or females) when exogenous testosterone is administered to support sexual activity. Similarly, there are no reports that aggression increases in hirsute females even though testosterone levels may rise to 200% above normal. Conversely, castration or antiandrogen administration to human males is not associated with a consistent decrease in aggression. Finally, changes in human aggression associated with neuropathology are not consistent with current knowledge of the neural basis of testosterone-dependent aggression. In contrast, human aggression does have a substantial number of features in common with defensive aggression seen in nonprimate mammals. It is present at all age levels, is displayed by both males and females, is directed at both males and females, and is not dependent on seasonal changes in hormone levels or experiential events such as sexual activity. As would be expected from current knowledge of the neural system controlling defensive aggression, aggression in humans increases with tumors in the medial hypothalamus and septal region, and with seizure activity in the amygdala. It decreases with lesions in the amygdala. The inference that human aggression has its roots in the defensive aggression of nonprimate mammals is in general agreement with evidence on the consistency of human aggressiveness over age, with similarities in male and female aggressiveness in laboratory studies, and with observations that some neurological disturbances contribute to criminal violence. This evidence suggests that human aggression has its biological roots in the defensive aggression of nonprimate mammals and not in hormone-dependent aggression based on testosterone.

Hormone-dependent aggression in male and female rats: experiential, hormonal, and neural foundations.

Hormone-dependent aggression in both male and female rats includes the distinctive behavioral characteristics of piloerection and lateral attack. In males the aggression is dependent on testicular testosterone and is commonly known as intermale aggression. In females, the aggression is most commonly observed as maternal aggression and is dependent on hormones whose identity is only beginning to emerge. The present review examines the experiential events which activate hormone-dependent aggression, the relation of the aggression to gonadal hormones, and the neural structures that participate in its modulation. In males and females, the aggression is activated by cohabitation with a conspecific of the opposite sex, by competitive experience, and by repeated exposure to unfamiliar conspecifics. In the female, the presence of pups also activates aggression. In both males and females, hormones are necessary for the full manifestation of the aggression. The essential hormone appears to be testosterone in males and a combination of testosterone and estradiol in females. The information available suggests the neural control systems for hormone-dependent aggression may be similar in males and females. It is argued that hormone-dependent aggression is behaviorally and biologically homologous in male and female rats.

Septal hyperreactivity: a comparison of lesions within and adjacent to the septum.

Following large septal lesions, male hooded rats were tested for reactivity 2, 7, and 14 days postoperatively. The results showed that lesions which destroyed the septal nuclei bilaterally caused a significant increase in reactivity above that of an operated control group. A similar increase in reactivity was produced by lesions which damaged the bed nucleus of the stria terminalis as well as the septum. A significantly greater level of reactivity was produced when the lesion destroyed the septum and in addition the area ventral to the anterior septum, including parts of the diagonal band of Broca and the accumbens nucleus. A second experiment examined the effectiveness of more restricted lesions ventral to the septum on reactivity. Ventral lesions which destroyed primarily the bed nucleus of the stria terminalis caused a small but significant increase in reactivity. With lesions ventral to the anterior septum the increase in reactivity was significantly larger. The increase in reactivity produced by the anterior-ventral lesions was also larger than that produced by lesions of the septum but it was not as great as that produced by combined lesions of the septum and the anterior-ventral area. These results suggest that several areas contribute to the hyperreactivity that is usually attributed to septal lesions.

Testosterone removal in rats results in a decrease in social aggression and a loss of social dominance.

Alpha male rats from mixed sex colony groups were tested for aggressiveness toward nonaggressive male intruders. Afterward, they were castrated and implanted with testosterone filled Silastic tubes, castrated and implanted with empty tubes, or sham castrated and implanted with empty tubes. There were significant declines in the aggressiveness (lateral attacks, bites, and piloerection but not on-top) of castrated rats without testosterone replacement but not in castrated rats with testosterone replacement. At a second operation, castrated animals had their testosterone capsules removed or had their empty capsules replaced with testosterone filled capsules. When tested for aggression toward nonaggressive intruders, those alpha males which had testosterone removed declined in aggressiveness while those which had it implanted returned to a level of aggressiveness close to that emitted by sham castrated control animals. Subordinate males became dominant when alpha males were castrated and not given testosterone replacement. In a final series of observations, sham castrated males were found to be more aggressive than castrated males when pitted against one another. It is argued that testosterone plays a primary role in intermale social aggression and that the decline in aggressiveness following castration is typically accompanied by a loss of social dominance.

The septal forebrain and the inhibitory modulation of attack and defense in the rat. A review.

Lesions of the septal region produce a dramatic change in behavior that is commonly known as septal rage. The present review of the literature indicates that this behavioral change occurs following damage to the lateral septum or to the region ventral to the anterior septum. Analysis of the behaviors resulting from lesions in these areas indicates that there is an increase in defensiveness and an increase in the tendency to attack. The increased defensiveness is seen in the enhanced reactivity to the human experimenter or in the shock-induced fighting situation, while the increased tendency to attack is seen most clearly in enhanced mouse and rat pup killing. The tendency for eating of the prey to occur suggests that the attack may have a predatory origin. Inconsistent effects have been reported on behavior in social situations. The lesion-induced changes in behavior are influenced by both pre- and postoperative experience and occur in many species in addition to the rat. They do not appear to be mediated by a cholinergic, dopaminergic, noradrenergic, or glutaminergic system. It is argued that most of the existing evidence can be accounted for if the septal forebrain region is considered to exert an independent inhibitory control over attack and defense.

Interanimal aggression and hyperreactivity following hypothalamic infusion of local anesthetic in the rat.

Abstract Temporary lesions were made by infusing a local anesthetic, lidocaine (2%), into the medial hypothalamus or adjacent areas of male hooded rats. Bilateral infusions of 1 μl, at a rate of 1 μl/3 min, were made every 5 min over a 20 min period. Reactivity to the experimenter, muricide, and intermale aggression were assessed following each 1 μl injection. Each of these behaviors was produced by injections along the descending columns of the fornix, in the anterior one-third of the ventromedial hypothalamic nucleus, and more posteriorly between the ventromedial nucleus and the fornix. The appearance of hyperreactivity, muricide, and intermale aggression were corelated with one another. The time of their appearance during the infusion period was similar for different infusion sites along the anterior-posterior length of the medial hypothalamus. Infusion of lidocaine into the medial forebrain bundle did not induce an increase in the behaviors measured. It is suggested that two systems, one modulating interanimal aggressiveness and another modulating reactivity (defensiveness) are being affected by these injections. The systems, while distinct, overlap in the medial hypothalamus. They are not localized solely in the ventromedial nucleus.

Hormone-dependent aggression in male rats is proportional to serum testosterone concentration but sexual behavior is not

Male hooded rats were castrated and implanted with Silastic capsules (1.57 mm i.d.; 3.18 mm o.d.) having a testosterone-filled space 0, 7, 22, 60, or 90 mm long. All animals were returned to their original group cages for a three-week period to allow hormone concentrations and behavioral tendencies to stabilize. Each male was then housed with an intact female in a large cage. Aggression by the male toward an unfamiliar male was tested at weekly intervals for three weeks. Sexual behavior with an estrogen/progesterone-primed ovariectomized female was tested on each of the subsequent two weeks. Serum testosterone was measured during the following week. The frequency of aggression was correlated with serum testosterone concentration up to the normal level and did not increase with higher serum testosterone concentrations. In contrast, sexual behavior was virtually absent in animals with no testosterone replacement and normal in all other groups. These results demonstrate a clear dissociation in the dependence of hormone-dependent aggression and sexual behavior on serum testosterone concentration. In a male cohabiting with a female, sexual experience activates hormone-dependent aggression toward an unfamiliar male but the level of aggression that develops depends on the serum testosterone concentration in the resident male.

An examination of the functionally effective spread of 4 μl of slowly infused lidocaine

Infusions of 4 μl of the local anesthetic lidocaine (2%) over a 15-min period were made in or adjacent to the oculomotor nucleus of the brain stem in an attempt to establish the functionally effective spread of the lidocaine. Infusions consistently produced complete ipsilateral dilation only when made within 0.5 mm of the ipsilateral nucleus. Complete contralateral dilation occurred only when the infusions were made within 0.25 mm of the center of the contralateral nucleus. These results agree with previous behavioral indications that slow infusion of relatively large volumes of the local anesthetic lidocaine do not produce a functional block over as large an area as would be predicted from volume considerations alone.

Serum estradiol concentration required to maintain body weight, attractivity, proceptivity, and receptivity in the ovariectomized female rat

Female hooded rats (230 to 260 g) were ovariectomized and given a subcutaneous implant of an estradiol-filled Silastic tube. The length of the tube was varied in order to produce a variety of serum estradiol levels. In the first experiment, animals were weighed over a 6-week period following surgery and then tested for sexual responsiveness to a male. The results demonstrated that ovariectomized females with an implant maintaining a serum estradiol concentration at about 15 pg/ml maintained body weight at the same level as that of intact females. A smaller implant gave rise to a higher weight gain and a larger implant to a lower weight gain. All implants resulted in a continuous state of receptivity. In a second experiment, ovariectomized females were implanted with smaller estradiol-filled implants in order to determine the threshold for maintaining proceptivity and receptivity. The results indicated that with a serum estradiol concentration below 15 pg/ml, the frequency of lordosis and of ear wiggling and darting decreased. Progesterone injections facilitated both proceptive and receptive behavior. In addition, following progesterone injections, the time required for a male to mount a female 10 times was decreased in females with low or no estradiol replacement. These results indicate that a constant concentration of estradiol at about the mean level present throughout the estrous cycle will result in normal body weight regulation and will maintain sexual behaviors that normally occur only during estrus. These results emphasize that Silastic implants of estradiol do not mimic normal endocrine function since, even at low levels, estradiol implants produce continuous receptivity.

Mouse killing and hyperreactivity following lesions of the medial hypothalamus, the lateral septum, the bed nucleus of the stria terminalis, or the region ventral to the anterior septum.

Abstract Electrolytic lesions in the medial hypothalamus, the lateral septum, or the region ventral to the anterior septum induced home cage mouse killing in 85 to 100% of rats when tested 2 days postoperatively and in 50 to 70% when tested at 21 days. When tested in a novel and larger test chamber, 100% of the rats with medial hypothalamic lesions killed mice at 2 days postoperatively but only 30% killed at 21 days postoperatively. Ten to thirty percent of animals with lesions of the lateral septum or of the region ventral to the anterior septum killed at any time in the novel environment. Lesions of the stria terminalis produced a slight increase in mouse killing in both the home cage and the novel environment. A high level of reactivity was produced by lesions of the medial hypothalamus, the lateral septum or the region ventral to the anterior septum but only that caused by the medial hypothalamic lesions was sustained over the 21 day test period. These results support previous evidence that the lateral septum, the region ventral to the anterior septum, and the medial hypothalamus are each important areas modulating mouse killing.