Information flow through threespine stickleback networks without social transmission.

Social networks can result in directed social transmission of learned information, thus influencing how innovations spread through populations. Here we presented shoals of threespine sticklebacks (Gasterosteous aculeatus) with two identical foraging tasks and applied network-based diffusion analysis (NBDA) to determine whether the order in which individuals in a social group contacted and solved the tasks was affected by the group's network structure. We found strong evidence for a social effect on discovery of the foraging tasks with individuals tending to discover a task sooner when others in their group had previously done so, and with the spread of discovery of the foraging tasks influenced by groups' social networks. However, the same patterns of association did not reliably predict spread of solution to the tasks, suggesting that social interactions affected the time at which the tasks were discovered, but not the latency to its solution following discovery. The present analysis, one of the first applications of NBDA to a natural animal system, illustrates how NBDA can lead to insight into the mechanisms supporting behaviour acquisition that more conventional statistical approaches might miss. Importantly, we provide the first compelling evidence that the spread of novel behaviours can result from social learning in the absence of social transmission, a phenomenon that we refer to as an untransmitted social effect on learning.

Complete maternal deprivation affects social, but not spatial, learning in adult rats.

The effects of maternal deprivation on learning of social and spatial tasks were investigated in female adult rats. Pups were reared artificially and received "lickinglike" tactile stimulation (AR animals) or were reared with their mothers (MR animals). In adulthood, subjects were tested on paradigms of spatial learning and on paradigms involving learning of social cues. Results showed that maternal deprivation did not affect performance on spatial learning, but it did impair performance on the three social learning tasks. The AR animals made no distinction between a new and a previously presented juvenile conspecific. AR animals also responded less rapidly than MR animals at test for maternal behavior 2 weeks after a postpartum experience with pups. Finally, AR animals did not develop a preference for a food previously eaten by a familiar conspecific whereas MR animals did. This study indicates that animals reared without mother and siblings show no deficits in spatial tasks while showing consistent deficits in learning involving social interactions.

Age-related changes in paternal responses of gerbils parallel changes in their testosterone concentrations.

Results of previous studies in our laboratory have shown that testosterone (T) inhibits parental response in adult male Mongolian gerbils. Here, we examined developmental changes in parental responses of male gerbils before, during, and after a naturally occurring surge in T that peaks on Day 75 postpartum. On the hypothesis that T inhibits parental response in male gerbils, we predicted that (a) 75-day-old male gerbils would be less responsive to neonates than would either younger or older male gerbils, and (b) young male gerbils whose T titers were rising as the litters that they were helping to rear matured would show a decrease over days in parental effort relative to older male gerbils whose T titers were falling as the litters that they were helping to rear matured. Both predictions were confirmed, providing evidence consistent with the view that naturally occurring, developmental changes in circulating concentrations of T play a role in age-related changes in the level of parental response of male Mongolian gerbils.

Effects of consanguinity, exposure to pregnant females, and stimulation from young on male gerbils' responses to pups.

In three experiments investigating variables affecting responses of male Mongolian gerbils to conspecific young, we compared the behavior directed towards pups of natural fathers, virgin foster fathers, and sexually experienced foster fathers (Experiment 1); males either previously exposed or not exposed to pregnant females (Experiment 2); and males provided or not provided with extra opportunities to huddle over pups (Experiment 3). We found no difference in responses to pups among natural fathers, virgin foster fathers, and foster fathers that had fathered litters. On the other hand, both a week of exposure to a pregnant female and opportunity to huddle over pups for an extra 15 min/day had significant effects on males' subsequent responses to conspecific young. We speculate on the reasons why a male's response to pups might be affected by his exposure to a pregnant female and stimuli from pups, but not by the probability that the pups were his own offspring.

Effects of caloric, protein, and sodium deprivation on the affiliative behavior of Norway rats (Rattus norvegicus).

The tendency of food-deprived, protein-deprived, and sodium-deprived Norway rats (Rattus norvegicus) and their respective controls to affiliate with conspecifics deprived of either food, protein, or sodium was examined. The authors found that (a) independent of internal state, focal rats offered a forced choice between protein-deprived and protein-replete target rats spent more time near replete than deprived target rats; and (b) both food-deprived and sodium-deprived focal rats offered a forced choice between food-deprived and replete target rats spent less time near fasted rats than did well-fed and sodium-replete focal rats. The data indicate that (a) rats can distinguish both food-deprived and protein-deprived rats from replete rats and (b) the deprivation states of rats can affect their willingness to affiliate with deprived conspecifics.

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.

Social influences on the amount of food eaten by Norway rats.

A naive observer Norway rat offered a choice between two foods, after it interacts with a demonstrator rat fed one of those foods, increases its preference for whichever food the demonstrator rat ate. It is not known whether interaction with a demonstrator rat would also increase the amount that an observer rat would eat if it were given access only to the food the demonstrator had eaten. In this study, each observer rat interacted with a demonstrator rat fed a food, either familiar or unfamiliar to the observer, and the observer was then offered a weighed sample of the food that the demonstrator had eaten. It was found that, during the first hour of testing, observer rats that had interacted with demonstrators fed an unfamiliar food, increased their intake of that food roughly four-fold. Observer rats that interacted with demonstrator rats fed a familiar food however, did not increase their food intake. Socially enhanced intake of unfamiliar food was seen only during the first hour that observers had access to food and was compensated for during the next 23 h of feeding. This short-term increase in observer intake of unfamiliar foods appeared to result from socially-induced motivation to ingest unfamiliar foods rather than from socially-induced reduction in neophobia.

Effects of experience on the parental responses of male Mongolian gerbils.

We examined responses of adult male Mongolian gerbils to nest site and young during the hours preceding and days following birth of a litter. We found that (a) male attendance at the nest site was markedly reduced for several hours following the birth of pups; (b) this lack of contact by males with nest and pups did not result from active exclusion of males from the nest by their mates; (c) males lacking previous experience of pups, but not those familiar with pups, avoided contact with pups on the day of their birth; and (4) 3-day-old gerbil pups were attractive even to males encountering young for the first time.

Demonstration of a socially transmitted flavor aversion in rats? Kuan and Colwill (1997) revisited.

In each of three experiments that differed only in procedural detail, observer rats interacted with pairs of conspecific demonstrators, one fed a cocoa-flavored diet (Diet Coc) and the other a cinnamon-flavored diet (Diet Cin). Immediately after both members of a pair of demonstrators had been fed, and 5 min before they interacted with an observer or observers, one of the demonstrators was made ill by intraperitoneal injection with lithium chloride. After interacting with a pair of demonstrators for 15 min, each observer was allowed to choose between Diet Cin and Diet Coc for 22 h. In all three experiments, observer rats consumed as much Diet Cin after interacting simultaneously with both an ill demonstrator that had eaten Diet Cin and a healthy demonstrator that had eaten Diet Coc as after interacting simultaneously with both a healthy demonstrator that had eaten Diet Cin and an ill demonstrator that had eaten Diet Coc. These results raise questions about the generality of Kuan and Colwill's (1997) demonstration of socially transmitted flavor aversions in Norway rats.

A testosterone-mediated trade-off between parental and sexual effort in male mongolian gerbils (Meriones unguiculatus).

Effects of testosterone (T) on parental behavior of male Mongolian gerbils (Meriones unguiculatus) were examined. After undergoing gonadectomy, castrated males were implanted with empty capsules or capsules containing T; sham-operated males were implanted with empty Silastic capsules. Subsequently, each male was paired with a pregnant female, and after delivery, families were observed 15 min/day for 20 days. Gonadectomized males without T spent more time in contact with, huddling over, and licking pups than did either sham-operated males or gonadectomized males with T. When given a choice between nest sites and displaced pups, females and males with low T preferred pups, whereas intact males and castrated males with T preferred nest sites. The findings are consistent with E. D. Ketterson and V. Nolan's (1994) hypothesis implicating T in mediating trade-offs between parental and sexual effort.

Environmental enrichment for laboratory rodents: animal welfare and the methods of science.

Because of the difficulty of' establishing objective measures of laboratory rodents' psychological well-being, developing environmental enrichment programs that are actually beneficial to rodents destined to participate in laboratory research is particularly challenging. Many studies of effects of environmental complexity, social housing, and increases in cage size suggest that professional judgments as to the impact of diverse types of environmental enrichment on rodent welfare are not a reliable basis for evaluating the outcomes of enrichment programs for laboratory rodents. Successful enrichment programs will vary from one rodent species to another, between sexes, as well as between age classes. There is a need for objective, measurable goals for proposed environmental enrichment programs for rodents, as well a s for empirical investigations of the beneficial and detrimental consequences of proposed environmental manipulations.

Effects of gonadectomy in infancy and adulthood on handedness in male and female Mongolian gerbils.

When assuming a species-typical tripodal posture, female Mongolian gerbils most often rest on their left forepaws and hold their right forelimbs aloft; male gerbils most often do the reverse. This experiment examined effects of gonadectomy, both in infancy and in adulthood, on the sexually dimorphic asymmetry in forelimb use by Mongolian gerbils when maintaining a tripodal stance. In adulthood, both male and female gerbils that had been gonadectomized at birth reversed their forelimb use while in a tripodal stance: Gonadectomized males used their forelimbs as did sham-operated females, and gonadectomized females used their forelimbs as did sham-operated males. Gonadectomy in adulthood abolished the sexual dimorphism in forelimb use seen in sham-operated subjects. It was concluded that gonadal hormones have organizational as well as possible activational effects on adult patterns of forelimb use by gerbils.

Intrauterine position, parenting, and nest-site attachment in male Mongolian gerbils.

We housed male Mongolian gerbils, their mates, and foster litters of standardized size and sex ratio in enclosures that provided cover in two locations. Males had been gestated in known intrauterine positions: either between two females (2F males) or between two males (2M males). From Days 1 to 20 postpartum, we examined the frequency with which both males and females were in contact with the pups they were rearing. We found that 2F males spent more time with pups than did 2M males both during entire observation periods and when females were away from the nest. Further, when pups were moved from the nest site. 2M males spent more time than did 2F males in the vacated nest site. We concluded that 2F male gerbils spent more time with pups than 2M males not because of a greater attachment of 2F than 2M males to places of concealment, their male, or their nest site. Rather, 2F males were more attracted to pups than were 2M males.

Effects of intrauterine position on the metabolic capacity of the hypothalamus of female gerbils.

The intrauterine position that a rodent fetus occupies relative to members of the same or opposite gender affects both its reproductive physiology and behavior when adult. Cytochrome oxidase histochemistry was used to assess regional differences in the oxidative metabolic capacity of the hypothalamus of female Mongolian gerbils that developed in utero between 2 female fetuses (n = 15) or between 2 male fetuses (n = 14). Cytochrome oxidase reactivity was measured densitometrically by experimenters unaware of subject intrauterine position. Gray-to-white matter ratios of optical density in 11 brain regions were used as a normalized index of metabolic capacity. Significant group differences in the metabolic capacity of the medial and the posterior parts of the anterior hypothalamus were revealed. Females that developed in utero between 2 male fetuses showed significant increases (19-22%) in cytochrome oxidase reactivity in these brain regions compared to that in females that developed between 2 female fetuses. The medial part of the anterior hypothalamus contributes to copulatory behavior, whereas the posterior part of the anterior hypothalamus may be involved in the control of pituitary gonadotropin secretion. Both these functions are influenced by intrauterine position during fetal life. To our knowledge, this is the first demonstration of metabolic changes in hypothalamic areas of the adult related to the differences in intrauterine position.

Reproductive profiles of adult Mongolian gerbils gestated as the sole fetus in a uterine horn.

We compared reproductive profiles of Mongolian gerbils gestated alone in a uterine horn (Isolate males and Isolate females) with those of gerbils gestated in intrauterine positions between two male fetuses (2M males and 2M females) and two female fetuses (2F males and 2F females). We found that, when adult, the reproductive profiles of gerbils that had been gestated as isolates resembled that of gerbils that had been gestated as 2F fetuses: 1. Isolate females gestated litters containing both the same proportion of males as the litters of 2F females and a significantly smaller proportion of males than litters of 2M females. 2. Isolate males, like 2F males, were less likely to impregnate females than were 2M males, and 3. both 2F males and isolate males exhibited disturbed patterns of copulation and reduced levels of scent-marking relative to 2M males. Our results were entirely consistent with the view that intrauterine exposure to males, but not to females, was responsible for previously described differences in the reproductive profiles of 2M and 2F Mongolian gerbils.

Interaction with demonstrator rats changes observer rats' affective responses to flavors.

The authors examined whether exposing naive rats (observers) to recently fed conspecific demonstrator rats changed the observers' later affective responses to foods their demonstrators ate. In Experiment 1, observers learned an aversion to a flavored fluid, then interacted with demonstrators that had drunk that fluid. These observers, but not those interacting with demonstrators that had drunk water, increased their intake of the averted fluid and exhibited fewer negative responses when the averted fluid was infused into their mouths. Rats in Experiment 2 entered the arm of a T maze known to lead to banana-flavored pellets more frequently after interacting with demonstrators fed banana-flavored pellets than after interacting with demonstrators fed chow-flavored pellets. Results of both experiments indicated that interaction with demonstrator rats changed observer rats' affective responses to flavors.

Sex and intrauterine position influence the size of the gerbil hippocampus.

Sex differences in home range size and spatial ability are predictive of sex differences in the relative size of the hippocampus in rodents. Such differences in behavior and hippocampal volume are presumed to be, in part, the result of differences in perinatal exposure to hormones. We predicted from differences in the size of home ranges of male and female Mongolian gerbils (Meriones unguiculatus) in the wild that the hippocampus of male gerbils would be relatively larger than that of females. We examined the effect of prenatal hormonal influences on hippocampal size by comparing hippocampal volume of males and females from 2F and 2M intrauterine positions to that of randomly selected males and females. We found that, as predicted, randomly selected males had a significantly larger hippocampus, relative to telencephalon, than did randomly selected females. However, males and females from 2F and 2M intrauterine positions did not differ in relative hippocampal size. Possible explanations for the absence of a sex difference in hippocampal size in male and female gerbils from 2F and 2M intrauterine positions are discussed.

Intrauterine position affects motoneuron number and muscle size in a sexually dimorphic neuromuscular system.

The intrauterine position occupied by a rodent fetus influences the amount of testosterone to which it is exposed before birth. Animals that are gestated between two male fetuses (2M) are exposed to higher circulating levels of testosterone than are animals positioned between two female fetuses (2F) and there are reliable differences in the reproductive physiology and behavior of 2M and 2F animals when adult. To determine whether intrauterine position modifies development of the central nervous system, we examined the sexually dimorphic spinal nucleus of the bulbocavernosus (SNB) in male and female gerbils from known intrauterine positions. We found that adult 2M female gerbils had 16% more SNB motoneurons than did 2F females. 2M males did not differ from 2F males in SNB motoneuron number, but the bulbocavernosus muscle, which is innervated by SNB motoneurons, was approximately 50% larger in 2M than in 2F males. These data indicate that intrauterine position can influence the morphology of the sexually dimorphic SNB neuromuscular system.

Effects of perinatal testosterone on handedness of gerbils: support for part of the Geschwind-Galaburda hypothesis.

When assuming their species-typical tripodal stance, male Mongolian gerbils (Meriones unguiculatus) use their right forepaw for support more frequently than do females. This experiment determined whether, as N. Geschwind and A. M. Galaburda (1987) have proposed, the direction of such sexually dimorphic lateral asymmetry of forelimb use is affected by perinatal exposure to testosterone (TP). It was found that male gerbils injected with TP when 4 days old were significantly less likely to rest on their right forepaw when in a tripodal stance than were their oil-injected siblings. Female gerbils injected with TP when 6 days old were more likely than oil-injected controls to use their right forepaws for support. The findings demonstrate effects of perinatal exposure to TP on handedness in gerbils and suggest that the relationship between TP exposure and asymmetrical forelimb use is not always as direct as Geschwind and Galaburda's model suggests.

Food selection: problems in understanding how we choose foods to eat.

Understanding food selection will require considerably more than reductionist analyses of the internal workings of individual animals. To understand food choice we will have to examine not only the physiology and behavior of individuals, but also the biological and social environments within which individuals select items to ingest. The biological environment determines patterns of food availability and, over evolutionary time, provides selective pressures which shape sensory-affective responses to flavors, making them adaptive with respect to local conditions. Direct experience of the consequences of ingesting potential foods and interaction with conspecifics that have eaten various foods both affect food choices. These multiple influences, acting at different levels of organization, can bias food selection by individuals in either adaptive or maladaptive directions, depending on the characteristics of the environment in which feeding occurs. The need to understand the relationship between internal organization, individual and social experience and ecological demands may make food choice the most difficult of the core aspects of feeding behavior to analyze satisfactorily.