Social enrichment improves social recognition memory in male rats

The social environment is thought to have a strong impact on cognitive functions. In the present study, we investigated whether social enrichment could affect rats’ memory ability using the “Different Objects Task (DOT),” in which the levels of memory load could be modulated by changing the number of objects to be remembered. In addition, we applied the DOT to a social discrimination task using unfamiliar conspecific juveniles instead of objects. Animals were housed in one of the three different housing conditions after weaning [postnatal day (PND) 21]: social-separated (1 per cage), standard (3 per cage), or social-enriched (10 per cage) conditions. The object and social recognition tasks were conducted on PND 60. In the sample phase, the rats were allowed to explore a field in which 3, 4, or 5 different, unfamiliar stimuli (conspecific juveniles through a mesh or objects) were presented. In the test phase conducted after a 5-min delay, social-separated rats were able to discriminate the novel conspecific from the familiar ones only under the condition in which three different conspecifics were presented; social-enriched rats managed to recognize the novel conspecific even under the condition of five different conspecifics. On the other hand, in the object recognition task, both social-separated and social-enriched rats were able to discriminate the novel object from the familiar ones under the condition of five different objects. These results suggest that social enrichment can enhance social, but not object, memory span.     

Non-specific effect of fear conditioning and specific effect of social defeat on social recognition memory performance in female rats

The so called "emotion learning" literature describes the ability of distressing and aversive unconditioned stimuli to classically condition a learned avoidance response. In order to investigate the impact of experience with noxious stimuli in one conditioning context on learning and memory performance in a separate, non-aversively motivated task, juvenile recognition ability was examined in adult female rats exposed previously to one of two environmental stressors. In particular, experimental adult rats were either socially defeated by exposure to an aggressive conspecific rat or fear conditioned using single or multiple pairings with footshock prior to performance of the social recognition task. Experiment 1 established that repeated exposure to a single juvenile resulted in social memory formation reflected in decreased social investigation from the first to the second exposure. Experiment 2 documented that both single and multiple pairings of an environment with footshock produced robust freezing behavior (90-95% suppression of activity). In addition, fear conditioning produced a non-specific 5-60% increase in social investigation time in both single and multiple-pairing fear conditioned groups which confounded the ability of the social recognition measure to assess effects of fear conditioning on learning and memory performance per se. In contrast, Experiment 3 documented that when social recognition memory performance was impaired to 85% of control levels by imposition of a 2 h delay, exposure to a social defeat stressor reinstated optimal social recognition memory performance. These findings suggest that the after effects of fear conditioning include non-specific alteration of social investigation whereas exposure to conspecific aggression enhances subsequent social recognition memory.     

Developmental expression of defensive responses during exposure to conspecific adults in preweanling rats (Rattus norvegicus).

I examined preweanling rats' (Rattus norvegicus) expression of ultrasounds and secretion of ACTH when exposed to unfamiliar adult male rats or to their mothers. Pups at 7 days of age produced similar levels of ultrasonic vocalization near both unfamiliar males and mothers. However, these pups could discriminate familiar from unfamiliar adults because ACTH was significantly higher in pups near adult males than in those near mothers. At 14 days of age, pups avoided adult males but not their mothers; therefore, adult males represented a significant threat. Importantly, 14-day-old rats significantly reduced ultrasound production only when near adult males. Pups at 21 days of age no longer emitted ultrasounds when socially isolated or when near conspecific adults. In addition, 14- and 21-day-old rats produced similar elevated ACTH levels across stimulus conditions. Results show significant changes in preweanling rats' responses to conspecific adults.     

Long-term effects of footshock and social defeat on anxiety-like behaviours in rats: Relationships to pre-stressor plasma corticosterone concentration

We compared the consequences of two stressors, 'unnatural' inescapable footshocks (IFSs) and 'natural' social defeat (SD), on behaviours typically sensitive to stress [sucrose preference, open field (OF), elevated plus maze (EPM) and acoustic startle responses (ASRs)] and the association with pre-stressor plasma corticosterone concentration. After initial blood sampling, rats (n?=?20 per group) were exposed to either 10 IFSs (1?mA intensity, 5?s duration each) or to 1?h SD (defeat by an aggressive resident male rat and further exposure but separated in a small cage) or to control procedures (handling). Rats were tested once for ASR (day 19), while the other behavioural tests were applied once weekly for 3 weeks. Both stress groups showed short-lasting lowered sucrose preference, and in the EPM they showed shorter total distance moved, shorter distance moved on open arms and less time on open arms compared to controls. In the OF test, IFS rats showed shorter total distance moved up to 2 weeks after stress. The SD group showed shorter total distance moved in the OF, which was only significant 2 weeks after stress. Low pre-stressor plasma corticosterone concentration was only associated with defecation (IFS rats) and latency to enter open arms in the EPM (all low corticosterone subgroups, n?=?10 per subgroup). SD rats with high initial plasma corticosterone concentration showed enhanced ASR compared to the other subgroups with high initial plasma corticosterone concentration (n?=?9 per subgroup). The results indicate that footshock and SD, while generally leading to an increase in anxiety behaviours, represent qualitatively different stressors.     

Gender dimorphic effects of voluntary running in laboratory rats depends on maturational status

This study examined the effect of 24 hr per day wheel access on running, body weight, and food intake for 30- or 50-day-old male and female rats under ad lib feeding conditions. Food intake and body weight were also monitored in a control group housed without access to running wheels. A dimorphic effect was observed after wheel introduction in 50-day-old but not 30-day-old rats: A temporary decline in food intake and a lasting decrease in body weight occurred for active male rats in comparison to their sedentary controls, and wheel access facilitated food intake and preserved body weight gain in female rats in comparison to their sedentary counterparts. Hyperphagia in adult females is interpreted in terms of the evolutionary acquired advantage linked to their reproductive function.     

Gender dimorphic effects of voluntary running in laboratory rats depends on maturational status

This study examined the effect of 24?hr per day wheel access on running, body weight, and food intake for 30- or 50-day-old male and female rats under ad lib feeding conditions. Food intake and body weight were also monitored in a control group housed without access to running wheels. A dimorphic effect was observed after wheel introduction in 50-day-old but not 30-day-old rats: A temporary decline in food intake and a lasting decrease in body weight occurred for active male rats in comparison to their sedentary controls, and wheel access facilitated food intake and preserved body weight gain in female rats in comparison to their sedentary counterparts. Hyperphagia in adult females is interpreted in terms of the evolutionary acquired advantage linked to their reproductive function.     

Organisational effects of neonatal and pubertal testosterone on sexually differentiated behaviours in the open-field and head-dip apparatus

On days 1 and 4 after birth rats were injected with 100 μg of testosterone propionate (TP) or vehicle, and at 35 days of age they were injected intramuscularly with 400 μg of testosterone oenanthate (TO), a long acting androgen, or the vehicle. There were four groups (oil-oil, TP-oil, oil-TO, TP-TO), each group subdivided by sex. Females treated with testosterone neonatally or at puberty were masculinised or defeminised on adult open-field behaviours, being less active and rearing less than oil-oil females; the oil-TO group also defaecated significantly more than controls. The TP-TO female group was indistinguishable from the oil-TO group. In a second experiment, sex differences were found in head-dipping behaviour as well as in activity and rearing. Females treated with TP or TO reared less and defaecated more than controls, and TP also decreased activity, but neither hormone treatment affected head-dipping behaviour. There is thus a peripubertal as well as a neonatal period when testosterone can act organisationally to masculinise or defeminise female rats. Potentiation between effects of neonatal and pubertal androgens was found on female body weights. TO alone had no effect, but TP-TO females were significantly heavier than controls at 90 days of age and by 130 days of age the TP-oil group was also heavier than controls.     

Intermittent exposure to social defeat and open-field test in rats: acute and long-term effects on ECG,body temperature and physical activity

This study investigated the effects of exposure to an intermittent homotypic stressor on: (i) habituation of acute autonomic responsivity (i.e. cardiac sympathovagal balance and susceptibility to arrhythmias), and (ii) circadian rhythmicity of heart rate, body temperature, and physical activity. After implantation of a transmitter for the radiotelemetric recording of electrocardiogram (ECG), body temperature and physical activity, adult male rats (Rattus norvegicus, Wild Type Groningen strain) were repeatedly exposed (10 consecutive times, on alternate days) to either a social stressor (defeat by a con-specific, n = 15) or an open-field, control challenge (transfer to a new cage; n = 8). ECGs, body temperature and physical activity were continuously recorded in baseline, test and recovery periods (each lasting 15 min), at the 1st and 10th episodes of both defeat and open-field challenge. The circadian rhythms of heart rate, body temperature and physical activity were monitored before (5 days), during (16 days) and after (21 days) the intermittent stress protocol. This study indicates that there is no clear habituation of either acute cardiac autonomic responsivity (as estimated by means of time-domain indexes of heart rate variability) or arrhythmia occurrence to a brief, intermittent, homotypic challenge, regardless of the nature of the stressor (social or non-social). On the other hand, rats exposed to social challenge also failed to show adaptation of acute temperature and activity stress responsiveness, whereas rats facing open-field challenge developed habituation of activity and sensitization of temperature responses. Repeated social challenge produced remarkable reductions of the heart rate circadian rhythm amplitude (this effect being significantly greater than that produced by intermittent open-field), but only minor changes in the daily rhythms of body temperature and physical activity.     

Gastric pathology and aphagia following lateral hypothalamic lesions in rats: effects of preoperative weight reduction.

The body weights of male albino rats were reduced gradually to 80% of normal body weight by resricting food intake (dieting), and then the rats were given lateral hypothalamic (LH) lesions. Compared with rats of normal body weight sustaining similar brain lesions, the dieted group displayed a shorter period of postoperative aphagia and less gastric pathology. In a second experiment, a group of rats was reduced to 80% of normal body weight by withholding all food (fasting) and then given LH lesions. Compared with dieted rats sustaining similar brain damage, the fasted group displayed a longer period of post operative aphagia and greater gastric pathology. Since the duration of aphagia could be shortened or lengthened by simple manipulations of preoperative body weight, the adequacy of sensorimotor or motivational hypotheses to account for aphagia is questioned. The results are more consistent with the suggestion that gastric abnormalities produced by LH lesions inhibit eating.     

Weight Loss in Rats Produced by Running: Effects of Prior Experience and Individual Housing

To investigate factors affecting activity-based anorexia (ABA) or activity-stress (AS), rats were given 2-hr access to a running wheel immediately prior to their daily 1.5-hr food access during the light cycle. This produced a reduction in food intake, a steady increase in running, and a large drop in body weight with a prolonged delay before weight recovery began. Experiment 1 found that these effects were reduced in rats with prior experience of eating at this time of day. In contrast, prior experience of running in the wheel when on ad lib food enhanced these effects in Experiment 2, where a subsequent change for half the subjects to individual housing produced a further decrease in body weight. The latter factor was investigated from the outset of Experiment 3 and again individually housed rats showed greater weight loss than did group-housed rats. This experiment also found that in rats of the same age a low initial body weight predicts greater vulnerability to ABA. It was concluded that ABA results from activity-induced reduction of feeding, which prolongs adaptation to a new feeding schedule and is accentuated by social isolation.     

Cattle discriminate between familiar and unfamiliar conspecifics by using only head visual cues

Faces have features characteristic of the identity, age and sex of an individual. In the context of social communication and social recognition in various animal species, facial information is relevant for discriminating between familiar and unfamiliar individuals. Here, we present two experiments aimed at testing the ability of cattle (Bos taurus) to visually discriminate between heads (including face views) of familiar and unfamiliar conspecifics represented as 2D images. In the first experiment, we observed the spontaneous behaviour of heifers when images of familiar and unfamiliar conspecifics were simultaneously presented. Our results show that heifers were more attracted towards the image of a familiar conspecific (i.e., it was chosen first, explored more, and given more attention) than towards the image of an unfamiliar one. In the second experiment, the ability to discriminate between images of familiar and unfamiliar conspecifics was tested using a food-rewarded instrumental conditioning procedure. Eight out of the nine heifers succeeded in discriminating between images of familiar and unfamiliar conspecifics and in generalizing on the first trial to a new pair of images of familiar and unfamiliar conspecifics, suggesting a categorization process of familiar versus unfamiliar conspecifics in cattle. Results of the first experiment and the observation of ear postures during the learning process, which was used as an index of the emotional state, provided information on picture processing in cattle and lead us to conclude that images of conspecifics were treated as representations of real individuals.     

Preadaptation to the feeding schedule does not eliminate activity-based anorexia in rats

To test whether activity-based anorexia (ABA) still occurs after preadaptation to the feeding schedule, 20 rats were first exposed to a feeding schedule of one 90-min meal per day until adaptation occurred (measured by maintenance of stable body weight). Then, during ABA training, half the rats (wheel group) were confined in running wheels except during the daily meal, and half (cage group) were not. Wheel running suppressed feeding—that is, food intake in the wheel group was less than that in the cage group. Also, the rats in the wheel group lost weight, whereas those in the cage group did not. Wheel running increased over days. Thus, the defining characteristics of ABA were evident in rats that were not subjected to ABA training until after they had become well adapted to the feeding schedule. These findings support the view that the suppression of feeding produced by wheel running triggers the vicious circle of ABA. They also cast doubt on the hypothesis that activity-induced interference with adaptation to the feeding schedule plays a key role in causing ABA.     

Role of female aggression in prevention of infanticidal behavior in male common voles,Microtus arvalis (Pallas, 1779)

Infanticidal behavior of male common voles (Microtus arvalis) was investigated in relation to the age of unfamiliar pups. Sires from 18 pairs were removed after parturition of their offspring and replaced by unfamiliar males at different ages of the neonates. In group 1, containing six females with their offspring, the new male was introduced into the females' cages on day 1 after the parturition. In group 2 the new male was introduced on day 5 after parturition and in group 3 on day 9 after parturition. The male was removed after 3 days and the neonates recounted. Male common voles killed up to 100% of the neonates in litters containing neonates younger than 9 days by rapid bites to the head of the neonates (groups 1 and 2, mortality rates of 0.86 and 0.38). However, with older pups, a mortality rate of 0.06 was observed while 33% of the intruder males showed signs of injuries (group 3). These findings show that infanticidal behavior of male common voles represents one factor of pup mortality. The results are discussed in relation to changes in the degree of maternal aggression and in the context of the social system of the common vole for solving the conflict between postpartum estrous mating and infanticidal behavior of male common voles. Aggr. Behav. 23:293–298, 1997. © 1997 Wiley-Liss, Inc.     

Food stealing by young Norway rats (Rattus norvegicus)

Six experiments were undertaken to explore factors affecting young rats' (Rattus norvegicus) frequencies of stealing food from conspecifics when identical food is available in surplus. It was found that (a) rats would walk across a bed of pellets to steal the particular pellet a peer was eating, (b) frequency of stealing within a pair did not decrease over days, (c) rats stole unfamiliar foods more frequently than familiar foods, (d) younger rats stole from older rats more frequently than older rats stole from younger ones, (e) hungry rats stole more frequently than replete rats, and (f) rats that had stolen a pellet of unfamiliar food from an anesthetized conspecific subsequently exhibited an enhanced preference for that food. Results suggest that food stealing is a mode of active seeking of information about what foods to eat.     

Further Evidence that Social Interaction Reduces Conditioned Taste Aversions in Mice

Social interactions with other conspecifics affect food selection in mammals. A previous study suggested that male mice attenuate conditioned taste aversion (CTA) by lithium chloride after interacting with an unfamiliar male conspecific. The present study was designed to (a) examine whether interactions with a familiar conspecific would attenuate CTA and (b) investigate sex differences in the social attenuation of CTA in mice. Results indicated that interacting with a familiar conspecific of the same sex following poisoning attenuated conditioned taste aversions only in male mice. The results suggest that the familiarity of conspecifics was not a critical factor in the social attenuation of CTA. Discrepancies between present and previous findings are discussed.     

Familiarity and categorization in intergroup behavior

Several studies have shown that social categorization into groups, unaffected by other variables such as own interest, interpersonal relations, conflict of interests, previous hostility, etc., was a sufficient condition to induce discrimination against an outgroup. The purpose of the present study was to test the hypothesis that the subjects' uncertainty and insecurity in a novel situation was, at least in part, responsible for this phenomenon. Two groups of subjects were tested: one group was made familiar with the social and physical setting of the experiment in a situation closely resembling the actual experiment, and came back for a second session in which the actual experiment was conducted; the second group came only for the actual experimental session. The results clearly indicate that, contrary to the hypothesis, the “familiar” group engaged in more out-group discrimination than the “unfamiliar” one. The theoretical and methodological implications of this finding are discussed.     

Retrograde Enhancement of Human Kinesthetic Memory by Alcohol: Consolidation or Protection against Interference?

Alcohol intake is known to impair memory in animals and humans. However, five studies reported that “medium” (0.05 ml/kg body weight) to “high” (1.0 ml/kg body weight) doses of alcohol improved memory when drunk immediately after initial learning of verbal or visual material. It was proposed that alcohol brought about this retroactive facilitation either through enhanced consolidation of memory traces or by protecting against retroactive interference. The present double blind study compared the performances of an alcohol and a placebo group on a kinesthetic memory task before alcohol or placebo intake and at retest 1 h after consumption. A second experiment was identical to the first except that all subjects carried out two trials on a T maze in the hour between testing and retesting. The alcohol group in the first experiment performed significantly better than the placebo group at retest (p< .05) but this was not the case in the second experiment. Alcohol therefore enhanced performance on the kinesthetic memory task in the first experiment but may not have protected against the moderate interference from the T maze in the second. The low levels of alcohol could have had a stimulant effect on trace consolidation, perhaps via raised blood glucose levels.     

Insulin and glucagon as determinants of body weight set point and microregulation in rats

Seven adult male rats were observed for body weight and microregulation (feeding, drinking, and running patterns) after manipulation of insulin and glucagon levels. They received three injections per day for 3 days each week of 3 U of protamine zinc insulin, .25 mg of zinc glucagon, 50 microgram of protamine zinc somatostatin (SRIF), or protamine zinc vehicle. Diabetes was then induced with an iv injection of streptozotocin (65 mg/kg), and the injection schedule was repeated after the full diabetic syndrome emerged. In all rats whose insulin levels were increased relative to glucagon levels, body weight increased; in those whose glucagon levels were increased relative to insulin levels, body weight decreased. All injections except vehicle reduced meal sizes in both normal and diabetic rats, but only insulin increased the frequency of feeding. These effects could be predicted by the glucostatic theory of food intake regulation and are thus interpreted as supportive of this theory. These results also support the hypothesis that the relative concentration of insulin to glucagon is a regulator of body weight set point.     

Interactions among chronic cold, corticosterone and puberty on energy intake and deposition

We have shown that chronic cold stress strongly interacts with corticosterone (B) to determine subsequent regulation of the hypothalamo-pituitary-adrenal (HPA) axis responses to novel stress. These studies, using the same 2 sets of rats, show that chronic cold also interacts with B and testosterone on signals of energy balance. The two groups of rats differed in weight by 20% and in age by 2 weeks (44-59 days of age). Adrenalectomized rats, replaced with varying doses of B, were exposed to cold or served as controls. Food intake and body weight during the experiments and hormones, metabolites and fat depots were measured on day 5. B, but not cold, affected food intake in the younger rats; by contrast, cold, but not B, affected food intake in the older rats. Testosterone was higher in older control rats and was markedly depressed by cold; younger rats had lower testosterone that was minimally affected by cold. Weight gain decreased in all rats at room temperature with increasing B, whereas they all lost weight in cold independently of B. Cold stimulated and B inhibited interscapular brown adipose tissue DNA content (reflecting sympathetic stimulation of thermogenesis). B stimulated insulin, whereas cold inhibited leptin and insulin; B also increased white adipose tissue weight gain in controls and inhibited its loss in cold. Leptin was unrelated to white adipose tissue depots in older control rats but was strongly related to these stores in younger rats and in all rats in cold. We conclude that: 1. By decreasing signals that act centrally to inhibit food intake (insulin, leptin and testosterone) cold allows B to stimulate food intake; 2. B inhibits weight gain although it causes accrual of fat; 3. Cold, probably through sympathetic stimulation of white adipose tissue, causes fat loss which is modulated by the inhibitory effect of B on sympathetic outflow; and, 4. The slope of the relationship between fat depot size and leptin becomes flatter in cold, possibly because of increased sympathetic outflow to these depots.