David B. Adams

Brain mechanisms for offense, defense, and submission

A preliminary attempt is made to analyze the intraspecific aggressive behavior of mammals in terms of specific neural circuitry. The results of stimulation, lesion, and recording studies of aggressive behavior in cats and rats are reviewed and analyzed in terms of three hypothetical motivational systems: offense, defense, and submission. A critical distinction, derived from ethological theory, is made between motivating stimuli that simultaneously activate functional groupings of motor patterning mechanisms, and releasing and directing stimuli that are necessary for the activation of discrete motor patterning mechanisms. It is suggested that motivating stimuli activate pathways that converge upon sets of homogeneous neurons, called motivational mechanisms, whose activity determines the motivational state of the animal. A defense motivational mechanism is hypothesized to be located in the midbrain central gray. In addition to tactile, auditory, and visual inputs from the paleospinothalamic tract, lateral lemniscus, and (perhaps) from the pretectum, it may receive inputs from a major forebrain pathway whose functional significance is not yet understood. A submission motivational mechanism is also thought to be located in the central gray. In addition to inputs for defense, it is thought to receive a necessary input from a “consociate (social familiarity cue) modulator” located in the ventromedial hypothalamus, which can switch behavior from defense to submission. The location of the hypothetical offense motivational mechanism is not known, although the pathways by which it is activated are traced in some detail. Brain mechanisms of aggression in primitive mammals and in primates are apparently similar to those in rats and cats.

Rise in Female-Initiated Sexual Activity at Ovulation and Its Suppression by Oral Contraceptives

This study was designed to test the hypothesis that women exhibit peaks of sexual activity at ovulation, as would be predicted from estrous effects in animals. Married women who used contraceptive devices other than oral contraceptives experienced a significant increase in their sexual behavior at the time of ovulation. This peak was statistically significant for all female-initiated behavior, including both autosexual and female-initiated heterosexual behavior, but was not present for male-initiated behavior except under certain conditions of contraceptive use. Previous failures to find an ovulatory peak may be due to use of measures of sexual behavior that are primarily determined by initiation of the male partner. Women using oral contraceptives did not show a rise in female-initiated sexual activity at the corresponding time in their menstrual cycles, probably owing to the suppression of ovulatory increases in hormone secretion by the oral contraceptives.

The relation of scent-marking, olfactory investigation, and specific postures in the isolation-induced fighting of rats.

The temporal sequences of acts and postures of rats during tests for isolation-induced fighting were recorded and analyzed. Scent-marking and olfactory investigation, which have been related to fighting by previous studies, were particularly emphasized. From the data a model was constructed for the sequence of behaviors which lead to and maintain isolation-induced fighting. The typical sequence begins with olfactory investigation and scent-marking; the home rat initially investigates the intruder, and the intruder initially investigates the cage. The combination of olfactory perception of a strange male and a familiar environment, it was suggested, serves to trigger an offensive mechanism in the home rat which leads to bite-and-kick attack and offensive sideways posture. The pain of the attack then triggers defensive mechanism in the intruder rat which leads to defensive upright posture and submissive posture. Whereas the functional role of the bite-and-kick attack appears to be simply the infliction of pain and elicitation of defense in the intruder, the function of offensive sideways posture as a threat behavior may be more complex. It is possible that it becomes a conditioned pain stimulus due to its close temporal pairing with bite-and-kick attack, but it is more likely that it produces defense by a process of sensitization. In any case, following the initial attack, the offensive sideways posture continues to elicit defensive behavior by the intruder even when there are no further attacks. The functional roles of the defensive postures were interpreted as positioning the intruder in such a way that the home rat cannot assume the aggressive posture from which attack is launched. Scent-marking behavior was consistent within strains, within individuals, and across different types of measures (accumulation of scent-marking marking material and performance of the stereotyped scent-marking act, crawl-over-dish). Amount of scent-marking was not correlated with attack, however, and its role in isolation-induced fighting remains unclear. In parallel to findings in other rodents, it was observed that scent-marking was diminished in animals after they had been subjected to attack.

Motivational systems of agonistic behavior in muroid rodents: A comparative review and neural model

The data on agonistic behavior of muroid rodents that have been obtained from field observations and laboratory experiments are reviewed and compared in terms of a hypothetical model of the neural organization of these behaviors. The neural model has been presented elsewhere and is used here only as a way to organize the data. The data are organized in terms of four hypothetical motivational systems: Offense, defense, submission, and patrol/marking. The various behaviors are considered as motor patterns and are compared and analyzed in terms of the proposed motivating, releasing, and directing stimuli of the motivational systems. Interactions and overlaps between the motivational systems are also considered. It is concluded that the organization of agonistic behavior may be similar across all species of muroid rodents. Generalizations are complicated by the profound effects of ontogenetic factors. Four categories of behaviors differ from species to species: Scent-marking, submissive behaviors, threat behaviors, and alarm signals. The possible phylogenetic and ontogenetic factors in these differences are considered.

Role of midbrain central gray in pain-induced defensive boxing of rats.

Abstract Pain-induced defensive boxing behavior in the rat was impaired or abolished by lesions of the midbrain central gray at the level of the superior colliculus. Lesions which left part of this region intact along with its lateral and dorsal connections did not produce boxing deficits despite destruction of anterior, posterior, or ventral connections. On the basis of these data, consideration of the anatomy and physiology of the central gray, and comparison to data on affective defense in the cat, it was suggested that this region may function as a modal command system or a patterning mechanism independent of the forebrain for pain-induced defensive boxing in the rat and affective defense in the cat. The central gray was shown to be necessary for freezing and escape behaviors as well as pain-induced defensive boxing, which led to speculation about its role in committing the animal to one or another of these three alternative responses to pain or threat.

SINGLE UNIT RECORDING IN THE MIDBRAIN OF RATS DURING SHOCK-ELICITED FIGHTING BEHAVIOR

Single unit activity was recorded extracellularly from the midbrain of rats during fighting behavior and during non-fighting control manipulations. Fighting behavior was elicited by footshock or startle stimuli or occurred spontaneously as a result of prior footshock presentations. Seven cells were found in the midbrain reticular formation and central gray which displayed maximum firing rates during fighting behavior. These cells also fired to a limited extent to some of the control manipulations, particularly contralateral vibrissae stimulation. These cells fired phasically during fighting behavior and their firing was correlated with either the approach or paw-strike of the opponent animal or to the response of the recording animal to a tactic of the opponent animal. However, no specific movement or sensory event reliably predicted the firing of these cells during fight sequences. Cells located in other midbrain areas, such as the deep tectum or the area of the red nucleus, also responded during fighting behavior. However, the discharge of these cells was correlated with specific body movements or sensory events. The activity during fighting was similar in rate and pattern to activity during control manipulations whenever similar movements or sensory stimulation were produced. Cells were also found which did not discharge during fighting behavior although they fired under a variety of other conditions.

Brain mechanisms of aggressive behavior: An updated review

During the 25 years since a motivational systems model was proposed to explain the brain mechanisms of aggressive behavior (D.B. Adams. Brain mechanisms for offense, defense, and submission. Behav. Brain. Sci. 2, (1979a) 200-241) considerable research has been carried out. Updating the model in the light of this research requires several changes. A previous distinction between submission and defense systems is abandoned and, instead, it is proposed that two distinct subsets of the defense motivational mechanism may be recognized, one for anti-predator defense and the other for consociate defense. Similarly, the offense motivational mechanism is now considered to have at least two subsets, one mediating territorial and the other competitive fighting. Data continue to indicate that the defense motivational mechanism is located in the midbrain central gray and adjoining tissue. Also data tend to support the hypothesis that the offense motivational mechanism is located in the hypothalamus at the level of the anterior hypothalamus. Consideration is also given to a motivational system for patrol/marking which is related to aggressive behavior. Research is reviewed that bears on the neural structure of motivating and releasing/directing stimuli and motor patterning mechanisms of offense, defense and patrol/marking, as well as the location of learning and hormonal effects, and attention is given to how the model can be tested.

Offense produced by chemical stimulation of the anterior hypothalamus of the rat

Offense behavior, including bite-and-kick attack, was obtained by microinjections of picrotoxin into the anterior hypothalamus of the rat. This is the first time that it has been possible to obtain offense by chemical stimulation of the brain, and the localization is more precise than that obtained with electrical stimulation. Mounting behavior and mounting by the opponent were also obtained from the anterior hypothalamus, the former corresponding to results obtained by previous studies using electrical stimulation. Other behaviors obtained from the hypothalamus included locomotion and circling, social and self-grooming, upright posture and boxing, digging, feeding, and leaping.

Ventrobasal thalamus necessary for visually-released defensive boxing of rat.

Abstract Visually-released, pain-induced defensive boxing in the rat was abolished by lesions which destroyed the ventrobasal thalamus. The visually-released boxing was produced by facial anesthesia of one of a pair of rats which were administered footshock in a small chamber; the rat with facial anesthesia was forced to rely upon visual stimuli rather than the facial tactile stimuli which normally release the behavior. The abolition of the visually-released boxing was specifically related to destruction of the ventrobasal thalamus rather than adjoining structures. A particularly effective control procedure involved abolition of the response by unilateral lesions confined to the ventrobasal thalamus and removal of visual input to the contralateral side of the brain by closure of the ipsilateral eye. Since visually-released boxing is a learned behavior dependent upon the visual cortex, it would appear that cortical mechanisms incorporate higher levels of the tactile projection system into an alternative system which releases the behavior after facial anesthesia.

ACTIVITY OF BASAL FOREBRAIN NEURONS IN THE RAT DURING MOTIVATED BEHAVIORS

The activity of single neurons in the basal forebrain was recorded in the freely-moving rat with moveable fine-wire electrodes. Neural activity was observed while the water-deprived male rat was exposed to three different types of motivating stimuli that elicit locomotion in a running wheel: an estrous female rat; a drinking tube containing water; and grasping and lifting by the experimenter. The neural activity was also observed when the subject was presented with standardized sensory tests and during single pulse stimulation of other brain structures. A majority of the 76 neurons recorded in the forebrain changed their firing rate during orienting and/or locomotion in general (23 neurons) or during behavior related to only one of the specific motivational contexts: the conspecific female (4 neurons); water (7 neurons); or grasp by the experimenter (8 neurons). Whereas the neurons related to orienting and/or locomotion in general were scattered through various brain structures, those neurons related to specific motivational contexts were concentrated in specific areas: the sexually dimorphic nucleus of the medial preoptic area (conspecific female); lateral septum (water); and lateral preoptic area (water and grasp). The present results, although based on relatively few neurons, are consonant with results of research using other techniques. This indicates that analyses at the level of the single neuron promise to be useful for understanding the role of the basal forebrain in motivational systems.