Jon L. Williams

Influence of shock controllability by dominant rats on subsequent attack and defensive behaviors toward colony intruders

Thirty colonies, each consisting of a female and two male adult albino rats, remained intact for an 8-week period. Naive conspecific intruders were then introduced into each colony for a 10-min test for 5 consecutive days. Videotapes of the tests were scored for aggressive and defensive behaviors. In every colony, aggression was greatest for a single alpha male. The alpha rats were randomly given one of three treatments: wheel-turn escape training, inescapable yoked shock, or restraint without shock. The alpha rats were then returned to their colonies and an intruder test was given 26 h later. Significant decreases in aggressive responses and increases in defensive behaviors occurred in the alpha yoked group but not in the other alpha groups. The nonalpha colony partners of the alpha yoked rats showed the opposite changes following the treatment. A final intruder test 72 h later revealed that the deficits in aggression of the alpha yoked group were still present but that the behaviors of most of the other groups were beginning to return to their respective pretreatment levels. These findings were discussed in terms of the concept of learned helplessness and alternative theoretical explanations.

A synthetic predator odor (TMT) enhances conditioned analgesia and fear when paired with a benzodiazepine receptor inverse agonist (FG-7142)

Benzodiazepine receptor inverse agonists, such as B-carboline-3-carboxylic acid n-methylamide (FG-7142), induce a state of fear and analgesia. These reactions can be conditioned to novel stimuli during drug administration. The present experiment was conducted to determine if FG-7142 is similar to other Stressors such that certain ethologically relevant stimuli are more likely to become conditioned to a state of fear than are others. 2,5-Dihydro-2,4,5-trimethylthiazoline (TMT), a compound previously isolated from the feces of the predator fox, and butyric acid (BA) were presented to male rats as novel odors after administration of FG-7142 or vehicle. A method of ensuring that equal amounts of these odors were presented to the subjects was employed. Six hours after one conditioning trial with drug or vehicle, the same nonodor or chemical odors were present during formalin tests for analgesia and fear-induced freezing. Compared with no-odor and BA groups, the TMT group showed significantly enhanced conditioned analgesia and fear when FG-7142 was administered during the conditioning session. However, relative to the other odor conditions, the TMT condition produced significantly higher levels of analgesia and freezing in the absence of the benzodiazepine inverse agonist, suggesting that this odor acts as an unconditioned Stressor by itself.

Influence of conspecific stress odors and shock controllability on conditioned defensive burying

In Experiment 1, rats received a session of 80 inescapable tail shocks or no shocks while restrained in a tube. During tests of conditioned defensive burying 24 h later, the bedding of the chamber contained odors from either stressed or nonstressed conspecific donor rats. Following a single prod shock, subjects that had had prior shocks or that were tested with the stress odors spent significantly less time burying the prod, made smaller piles of bedding, and displayed more freezing behavior. The combination of prior shock and stress odors during later testing enhanced these effects. In Experiment 2, a yoked group of rats that was given inescapable shocks, in contrast to a group that had wheel-turn escape training and one that was restrained but not shocked, later showed significantly less burying and more freezing when tested for defensive burying with stress odors present. In both experiments the duration of burying and the heights of piles were positively correlated, and both of these measures were negatively correlated with freezing. The demonstrated capacity of unconditioned stress odors to mediate different degrees of fear, depending upon the controllability of prior shock, is related to other studies of learned helplessness, and the predominance of freezing over burying is discussed in terms of various types of defensive strategies, stimulus-control processes, and the author’s stress-coping-fear-defense (SCFD) theory.

Influence of conspecific and predatory Stressors and their associated odors on defensive burying and freezing responses

In Experiment 1, male rats were exposed to either aggressive (i.e., alpha) or nonaggressive conspecific colonies and tested 24 h later, with or without alpha odors, for freezing behavior and burying of a wall prod that had been the source of a brief electric shock. The results indicated that prior defeat experience and the presence of alpha odors alone during testing had no significant effects, but the combination of prior defeat and alpha-odor testing significantly decreased burying and increased freezing behavior. In Experiment 2, we examined the effects of noncontact exposure to a cat, as a predatory Stressor, during subsequent prod-shock tests involving the presence or absence of cat odors. Exposure to a cat failed to disrupt later prod burying and did not produce freezing. However, the presence of cat odors during testing significantly reduced the amount of defensive burying,without resulting in an increment in freezing. In Experiment 3, rats were given 1, 5, or 30 inescapable preshocks in the presence of either cat odors or a hedonically neutral citronella odor and were tested 24 h later for prod burying and freezing with or without these odors. Both the cat and the citronella odors resulted in a significant reduction in burying and an increase in freezing for rats given 5 and 30 preshocks and tested in the presence of these respective conditioned odors. For the groups that were given 5 preshocks, preshock and later testing in the presence of cat odors resulted in significantly less prod burying and more freezing than for rats that were preshocked and tested in the presence of citronella. The findings of these three ethoexperimental studies are discussed in terms of the learned-helplessness theory, the stress-coping-fear-defense (SCFD) theory, and the concept of selective CS-US associability.

Effects of stress controllability, immunization, and therapy on the subsequent defeat of colony intruders

Three experiments investigated the influence that various stress-controllability manipulations had on the defensive behaviors of rats when they were subsequently tested as intruders in previously established, aggressive colonies of conspecifics. In Experiment 1, naive subjects that had received a session of 80 shocks in a tube showed an enhanced series of defensive responses and received more bites than did a group of restrained nonshocked rats as colony intruders 24 h later. These two measures were also found to be positively correlated within each group. In Experiment 2, a group that was given 80 yoked inescapable shocks, in contrast to a group that had wheel-turn escape training and a restrained nonshocked control group, displayed more defeat and was bitten more frequently when tested as intruders on the following day. In Experiment 3, 60 trials of wheel-turn escape training were given 4 h prior to (i.e., immunization) or after (i.e., therapy) a session of 60 inescapable tube shocks. During resident-intruder testing 24 h later, both of these groups showed less defeat and received fewer bites than did an inescapably preshocked group but did not differ from a restrained nonshocked control group. These findings clearly indicate that stress controllability alters species-typical defensive responses, and their implications concerning other learned helplessness effects and interpretations are discussed.

Exposure to uncontrollable stress alters withdrawal from morphine

Prior exposure to uncontrollable stress potentiates morphine analgesia. This study was designed to examine the influence of the controllability/uncontrollability of shock as a stressor on the severity of subsequent morphine withdrawal. In Experiment 1, rats that received two daily sessions of 80 yoked-inescapable shocks, in contrast to those given 80 escapable shocks or restrained without shock, showed an enhanced series of correlated withdrawal behaviors (i.e., mouthing, teeth chattering, and head/body shakes) 24 hr later when injected with morphine (5 mg/kg) followed by a naloxone (5 mg/kg) challenge. In Experiment 2, this finding was replicated with escape-yoked-restrained groups of rats given saline injections during the pretreatment phase, but the impact that only inescapable shock had on later precipitated withdrawal was completely blocked when subjects were administered naltrexone (14 mg/kg) before each shock session. These findings are discussed in terms of the capability of inescapable shock to activate an endogenous opiate system(s) and thereby lead to a sensitization of release or receptor processes which could potentiate later morphine withdrawal.

Effects of repeated defeat by a dominant conspecific on subsequent pain sensitivity, open-field activity, and escape learning

Male rats were tested as intruders for 25 consecutive days in colonies that had either aggressive (i.e., alpha) or nonaggressive conspecific residents. Alpha-defeated intruders, in contrast to nondefeated rats, showed more defensive behavior, less gain in body weight, and received more bites during the course of these sessions. Tail-flick tests, using a heat source, revealed that both groups of intruders showed comparable sensitivity/reactivity to pain, and there was no evidence of analgesia as a function of resident encounters. Immediately after the last intruder session, all subjects were tested for exploratory activity in an open-field apparatus with the odors (i.e., soiled bedding) from the alpha colonies present. Defeated intruders showed significantly less locomotion, in terms of the number of grid crossings, than nondefeated rats. Twenty-four hours later, randomly selected subgroups of defeated and nondefeated subjects were briefly exposed, without being defeated, to aggressive colonies, and all rats were then retested for activity with alpha odors present. Previously defeated intruders were again less active, and the colony-exposure treatment suppressed the activity of defeated, but not nondefeated, subjects. Finally, 24 h after another resident-intruder session, both groups of intruders showed comparable FR 1 escape performance in a shuttlebox with alpha odors present, but the defeated rats failed to learn a subsequent FR 2 escape task. The findings of this experiment are discussed in terms of the concept of “learned helplessness,” the effects of ethological stressors, and the authors’ stress-coping-fear-defense (SCFD) theory.

Defeat-induced hypoalgesia in the rat: effects of conditioned odors, naltrexone, and extinction.

In Experiment 1, male rats were either defeated as a colony intruder by alpha conspecifics or had no defeat experience, and 24 hr later they were given a paw injection of formalin prior to observational tests with or without alpha-colony odors. The combination of defeat and tests with these odors produced conditioned hypoalgesia (i.e., a suppression in paw licking) and freezing. In Experiment 2, defeated rats were given either an injection of naltrexone or saline prior to defeat and 24 hr later prior to testing. An injection of naltrexone prior to defeat increased freezing during defeat and later testing. In contrast, naltrexone during testing did not affect freezing but significantly reduced hypoalgesia. In Experiment 3, a 12-hr exposure session with alpha-colony odors extinguished hypoalgesia in previously defeated rats. These findings are discussed in terms of associative, opioid/nonopioid, and adaptive evolutionary processes.

Prolonged exposure to conspecific and predator odors reduces fear reactions to these odors during subsequent prod-shock tests

In Experiment 1, four groups of male rats were given a session as an intruder in either aggressive (i.e., alpha) or nonaggressive colonies of conspecifics and later received either a 2-h exposure to the odors of the alpha colonies or an exposure-control session with the odors of a nonalpha colony. Two additional groups of rats that had been attacked and defeated by alpha residents were later given a 12-h exposure session with alpha-colony odors or nonaipha-control odors. Twenty-four h after the colony-intruder session, all subjects were given a single 6.5-mA shock from a prod with alpha-colony odors present in the bedding of the test chamber. Attacked rats that had been given exposure-control sessions showed significantly less prod burying and greater freezing than nondefeated subjects. This implies that the alpha-colony odors elicited conditioned fear. In contrast, the attacked subjects that had been given a pretest exposure session with alpha-colony odors showed significantly more prod burying and significantly less freezing. This suggests that the alpha-odor exposure resulted in the extinction of fear to these odors. Furthermore, the 12-h exposure to alpha-colony odors was found to be more effective in reducing fear-mediated responses than was the 2-h exposure. In Experiment 2, three groups of rats were exposed to a cat while they were in a protective cage; later they were given a 12-h exposure session with cat odors, a 12-h exposure-control session with no cat odors, or no exposure treatment. Compared with the two control groups, the subjects that were exposed to cat odors showed less freezing during subsequent prod-shock tests in the presence of cat odors, but they did not show prod burying. The reported changes in fear-mediated reactions to the odors of conspecifics and a predator are discussed in terms of both associative and nonassociative processes.

Effects of cat exposure and cat odors on subsequent amphetamine-induced stereotypy

The effect of exposure to a cat, as a predatory stressor, was examined in male and female rats during subsequent tests of amphetamine-induced stereotypy in which cat odors were present or absent. Rats in Group C/O were given a 15-min exposure session to a male cat while they were protected in a wire cage. They were then given an IP injection of d-amphetamine (1 mg/kg) and tested 30 min later for stereotypy in the presence of cat odors (soiled cat litter). Rats in Group NC/O were given a no-cat-exposure control session, and amphetamine tested with cat odors. Groups C/NO and NC/NO were both tested without cat odors (fresh litter), with the former group having been previously exposed to a cat. During the 90-min test sessions, female rats showed significantly more stereotypy than males. More importantly, the male subjects in group C/O exhibited significantly more stereotypy than the males in the other groups, and group NC/NO males showed the least amount of stereotypy. These findings clearly indicate that amphetamine reactivity is influenced by prior exposure to a predator, the presence of predatory odors during testing, and the subjects sex.