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Lim, M. M., & Young, L. J. (2006). Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Hormon. Behav., 50(4), 506–517.
Abstract: Social relationships are essential for maintaining human mental health, yet little is known about the brain mechanisms involved in the development and maintenance of social bonds. Animal models are powerful tools for investigating the neurobiological mechanisms regulating the cognitive processes leading to the development of social relationships and for potentially extending our understanding of the human condition. In this review, we discuss the roles of the neuropeptides oxytocin and vasopressin in the regulation of social bonding as well as related social behaviors which culminate in the formation of social relationships in animal models. The formation of social bonds is a hierarchical process involving social motivation and approach, the processing of social stimuli and formation of social memories, and the social attachment itself. Oxytocin and vasopressin have been implicated in each of these processes. Specifically, these peptides facilitate social affiliation and parental nurturing behavior, are essential for social recognition in rodents, and are involved in the formation of selective mother-infant bonds in sheep and pair bonds in monogamous voles. The convergence of evidence from these animal studies makes oxytocin and vasopressin attractive candidates for the neural modulation of human social relationships as well as potential therapeutic targets for the treatment of psychiatric disorders associated with disruptions in social behavior, including autism.
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Thor, D. H., & Holloway, W. R. (1982). Social memory of the male laboratory rat. J. Comp. Physiol. Psychol., 96(6), 1000–1006.
Abstract: Used duration of social-investigatory behavior by 36 mature male Long-Evans rats as a measure of individual recognition in 5 experiments to assess social memory. In Exp I, the duration of social investigation during a 2nd exposure to the same juvenile (n[en space]=[en space]12) was directly related to the length of the interexposure interval. In Exp II, Ss were exposed to the same or different juvenile 10 min after an initial 5-min exposure to a novel juvenile; reexposure to the same juvenile elicited significantly less social investigation than an exposure to a different juvenile. Exps III and IV demonstrated that following a 5-min introductory exposure, social memory of the juvenile was relatively brief in comparison with that of mature Ss. Exp V revealed a retroactive interference effect on recently acquired memory for an individual: 12 mature Ss exposed to interpolated social experience engaged in significantly longer investigation of a juvenile than those with no interpolated social experience. The combined results suggest that (1) the rat normally engages in spontaneous learning of individual identity and (2) social memory may be a significant aspect of complex social interactions. (16 ref) (PsycINFO Database Record (c) 2006 APA, all rights reserved)
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Trillmich, F., & Rehling, A. (2006). Animal Communication: Parent-Offspring. In Keith Brown (Ed.), Encyclopedia of Language & Linguistics (pp. 284–288). Oxford: Elsevier.
Abstract: Parent-offspring communication has evolved under strong selection to guarantee that the valuable resource of parental care is expended efficiently on raising offspring. To ensure allocation of parental care to their own offspring, individual recognition becomes established in higher vertebrates when the young become mobile at a time when a nest site can no longer provide a safe cue to recognition. Such recognition needs to be established by rapid, sometimes imprinting-like, processes in animals producing precocial offspring. In parents, offering strategies that stimulate feeding and entice offspring to approach the right site have evolved. Such parental signals can be olfactory, acoustic, or visual. In offspring, begging strategies involve shuffling for the best place to obtain food – be this the most productive teat or the best position in the nest. This involves signals that make the offspring particularly obvious to the parent. Parents often feed young according to their signaling intensity but may also show favoritism for weaker offspring. Offspring signals also serve to communicate the continuing presence of the young and may thereby maintain brood-care behavior in parents. Internal processes in parents may end parental care irrespective of further signaling by offspring, thus ensuring that offspring cannot manipulate parents into providing substantially more care than is optimal for their own fitness.
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Levy, F., Keller, M., & Poindron, P. (2004). Olfactory regulation of maternal behavior in mammals. Horm Behav, 46(3), 284–302.
Abstract: In mammals, olfactory cues are extensively used in many aspects of maternal care to ensure the coordination of mother-infant interactions and consequently the normal development of the offspring. Outside the period of parturition and lactation, when the young are not a behavioral priority, olfactory cues play an inhibitory role on maternal responsiveness since in most mammalian species studied so far, nonpregnant females find the odor of young aversive. On the contrary at the time of parturition, a shift in the hedonic value of infantile odors occurs so that the young now become a very potent stimulus and this sensorial processing constitutes an important part of the maternal motivational system. Moreover, infants' odors provide a basis for individual recognition by their mothers and some species (ungulates) have developed highly specialized mechanisms for processing of the infant signals. Perception of the smell of the young also regulates various aspects of maternal behavior. Dodecyl propionate, a compound released by of pup's preputial glands, has been shown to influence anogenital licking behavior, a fundamental pattern of maternal behavior in rodents. While there is no functional specificity of either the main or the accessory olfactory systems in the development of maternal behavior amongst species, it appears that only the main olfactory system is implicated when individual odor discrimination of the young is required. Neural structures, such as the main olfactory bulb, undergo profound changes when exposed to offspring odors at parturition. These changes in synaptic circuitry contribute both to maternal responsiveness to these odors, to their memorization, and to effects of long-term maternal experience.
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Patris, B., Perrier, G., Schaal, B., & Coureaud, G. (2008). Early development of filial preferences in the rabbit: implications of nursing- and pheromone-induced odour learning? Anim. Behav., 76(2), 305–314.
Abstract: Newborn rabbits, Oryctolagus cuniculus, discriminate between different categories of adult conspecifics on the basis of their abdominal odour cues. Whether these cues can support the development of filial preferences has not been adequately tested. Using a two-choice paradigm, we assessed the ability of 3-8-day-old pups to orient selectively to the mother versus an unfamiliar female, either spontaneously or after odour conditioning. In experiment 1, nonconditioned pups roamed indifferently over the mother and an unfamiliar female. In experiment 2, pups conditioned to a neutral odorant while nursing or with the mammary pheromone became attracted by the odorant. In experiment 3, pups that had learned the odorant while nursing oriented for longer to any female carrying it, but the unscented mother and a scented unfamiliar female were equally attractive. Finally, in experiment 4, pups that had learned the odorant paired with the mammary pheromone showed a preference for their scented mother, but not systematically for a scented unfamiliar female; furthermore, they were equally attracted by the unscented mother and a scented unfamiliar female. In sum, pups did not spontaneously evince an olfactory preference for the mother when opposed to an unfamiliar female, although they seemed able to detect individual maternal odours. In fact, they appeared to react to both species-specific cues and individual cues that they had learned, and their responses depended on their degree of familiarity with the cues and on the context. The mammary pheromone by itself might act as both a releasing and a reinforcing signal in these early socially oriented behaviours.
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Lingle, S., Rendall, D., Wilson, W. F., DeYoung, R. W., & Pellis, S. M. (2007). Altruism and recognition in the antipredator defence of deer: 2. Why mule deer help nonoffspring fawns. Anim. Behav., 73(5), 907–916.
Abstract: Both white-tailed deer, Odocoileus virginianus, and mule deer, O. hemionus, females defend fawns against coyotes, Canis latrans, but only mule deer defend nonoffspring conspecific and heterospecific fawns. During a predator attack, females may have to decide whether to defend a fawn while having imperfect information on its identity obtained from hearing a few distress calls. Although imperfect recognition can influence altruistic behaviour, few empirical studies have considered this point when testing functional explanations for altruism. We designed a series of playback experiments with fawn distress calls to test alternative hypotheses (by-product of parental care, kin selection, reciprocal altruism) for the mule deer's defence of nonoffspring, specifically allowing for the possibility that females mistake these fawns for their own. White-tailed deer females approached the speaker only when distress calls of white-tailed deer fawns were played and when their own fawn was hidden, suggesting that fawn defence was strictly a matter of parental care in this species. In contrast, mule deer females responded similarly and strongly, regardless of the caller's identity, the female's reproductive state (mother or nonmother) or the presence of their own offspring. The failure of mule deer females to adjust their responses to these conditions suggests that they do not defend nonoffspring because they mistake them for their own fawns. The lack of behavioural discrimination also suggests that kin selection, reciprocal altruism and defence of the offspring's area are unlikely to explain the mule deer's defence of nonoffspring. We identify causal and functional questions that still need to be addressed to understand why mule deer defend fawns so indiscriminately.
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Lingle, S., Rendall, D., & Pellis, S. M. (2007). Altruism and recognition in the antipredator defence of deer: 1. Species and individual variation in fawn distress calls. Anim. Behav., 73(5), 897–905.
Abstract: Mule deer, Odocoileus hemionus, females actively defend fawns against predators, including nonoffspring conspecific fawns and heterospecific white-tailed deer, O. virginianus, fawns. We hypothesized that the defence of nonoffspring fawns was due to a recognition error. During a predator attack, females may have to decide whether to defend a fawn with imperfect information on its identity obtained from hearing only a few distress calls. We examined fawn distress calls to determine whether calls made by the two species and by different individuals within each species were acoustically distinctive. The mean and maximum fundamental frequencies of mule deer fawns were nearly double those of white-tailed deer fawns, with no overlap, enabling us to classify 100% of calls to the correct species using a single trait. A large proportion of calls was also assigned to the correct individual using a multivariate analysis (66% and 70% of mule deer and white-tailed deer fawns, respectively, chance = 6% and 10%); however, there was considerable statistical uncertainty in the probability of correct classification. We observed fawns approach conspecific females in an attempt to nurse; females probed most offspring fawns with their noses before accepting them, and always probed nonoffspring fawns before rejecting them, suggesting that close contact and olfactory information were needed to unequivocally distinguish nonoffspring from offspring fawns. Taken together, these results suggest that acoustic variation alone would probably be sufficient to permit rapid and reliable species discrimination, but it may not be sufficient for mothers to unequivocally distinguish their own fawn from conspecific fawns.
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Scordato, E. S., & Drea, C. M. (2007). Scents and sensibility: information content of olfactory signals in the ringtailed lemur, Lemur catta. Anim. Behav., 73(2), 301–314.
Abstract: The function of olfactory signalling in social species is less well understood than in asocial species. Consequently, we examined olfactory communication in the ringtailed lemur, a socially complex primate that retains a functional vomeronasal organ, has well-developed scent glands and shows a suite of scent-marking behaviour. To assess the information content of different types of scent gland secretions, we decoupled olfactory cues from the visual and behavioural modalities with which scent marking is normally associated. We presented male and female subjects (signal receivers) with a series of choice tests between odours derived from conspecific donors (signal senders) varying by sex, age, social status and reproductive condition. We additionally examined the influence of the receivers' reproductive state and familiarity with the signaller. The reproductive condition, social status and familiarity of senders and receivers affected signal transmission; specifically, male receivers attended most to the odours of conspecifics in breeding condition and to the odours of familiar, dominant animals. By contrast, females varied their responses according to both their own reproductive state and that of the sender. Based on male and female patterns of countermarking, we suggest that scent marking serves a function in intergroup spacing and intrasexual competition for both sexes, as might be expected in a female-dominant species. By contrast, minimal female interest in male odours counters a female mate choice function for scent marking in this species. Nevertheless, scent marks are critical to male-male competition and, therefore, may be subject to sexual selection.
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Christensen, J. W., Zharkikh, T., & Chovaux, E. (2011). Object recognition and generalisation during habituation in horses. Appl. Anim. Behav. Sci., 129(2-4), 83–91.
Abstract: The ability of horses to habituate to frightening stimuli greatly increases safety in the horse-human relationship. A recent experiment suggested, however, that habituation to frightening visual stimuli is relatively stimulus-specific in horses and that shape and colour are important factors for object generalisation (Christensen et al., 2008). In a series of experiments, we aimed to further explore the ability of horses (n = 30, 1 and 2-year-old mares) to recognise and generalise between objects during habituation. TEST horses (n = 15) were habituated to a complex object, composed of five simple objects of varying shape and colour, whereas CONTROL horses (n = 15) were habituated to the test arena, but not to the complex object. In the first experiment, we investigated whether TEST horses subsequently reacted less to i) simple objects that were previously part of the complex object (i.e. testing for object recognition) and ii) a novel object (new shape and colour, i.e. testing for object generalisation), compared to CONTROLS. In the second experiment we investigated whether TEST horses reacted to a change in object order and object location. Behavioural reactions to the object, latency to eat, total eating time and heart rate were recorded. Compared to CONTROLS, TEST horses reacted significantly less towards objects, which were previously part of the complex object (e.g. mean heart rate; P = 0.006), indicating object recognition. In contrast to our expectations, TEST horses also reacted significantly less towards the novel object (e.g. mean heart rate; P = 0.018), suggesting that they were capable of object generalisation. We also found that TEST horses showed an increase in exploratory behaviour when objects within the complex object changed order and location (both P < 0.001), whereas there was no increase in heart rate, indicating that the horses were not frightened by the changes. The results demonstrate that it is possible to increase object generalisation in horses by habituating them to a range of colours and shapes simultaneously. This knowledge greatly affects the way in which horses may be trained to react calmly towards frightening objects.
Keywords: Horse; Habituation; Object recognition; Generalisation
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Ligout, S., Porter, R. H., & Bon, R. (2002). Social discrimination in lambs: persistence and scope. Appl. Anim. Behav. Sci., 76(3), 239–248.
Abstract: Social recognition among familiar unrelated lambs was assessed in a series of tests. Lambs and their mothers were housed together in small groups for 1 week (Original groups; O) then reorganized into new groupings (Recent-groups; R) for the remainder of the experiment. During test series 1, lambs that were paired with a familiar O-group partner, from which they had been separated for 5 days, emitted fewer distress bleats than did those tested with an unfamiliar partner. This same effect was not evident when the test was repeated several hours later, indicating that the animals had become habituated to the testing procedures. Two days later, when given the choice between an O- versus a R-partner (test series 2), lambs did not display a preference for either of the stimulus lambs. However, in an additional two-choice test (test series 3) the subject lambs responded discriminatively to a recent familiar partner that was simultaneously present with an unfamiliar lamb. Overall, the results suggest that lambs are capable of developing discriminative relationships with age-mates from different sub-groups, and that such social discrimination persists over a separation period lasting at least several days. It is not clear whether lambs recognize several individual conspecifics per se or discriminate between members of higher order social categories (e.g. familiar versus unfamiliar individuals). Proximal and distal social discrimination may be mediated by different combinations of sensory modalities.
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