Recording Single Neurons' Action Potentials from Freely Moving Pigeons Across Three Stages of Learning

While the subject of learning has attracted immense interest from both behavioral and neural scientists, only relatively few investigators have observed single-neuron activity while animals are acquiring an operantly conditioned response, or when that response is extinguished. But even in these cases, observation periods usually encompass only a single stage of learning, i.e. acquisition or extinction, but not both (exceptions include protocols employing reversal learning; see Bingman et al.¹ for an example). However, acquisition and extinction entail different learning mechanisms and are therefore expected to be accompanied by different types and/or loci of neural plasticity.Accordingly, we developed a behavioral paradigm which institutes three stages of learning in a single behavioral session and which is well suited for the simultaneous recording of single neurons'' action potentials. Animals are trained on a single-interval forced choice task which requires mapping each of two possible choice responses to the presentation of different novel visual stimuli (acquisition). After having reached a predefined performance criterion, one of the two choice responses is no longer reinforced (extinction). Following a certain decrement in performance level, correct responses are reinforced again (reacquisition). By using a new set of stimuli in every session, animals can undergo the acquisition-extinction-reacquisition process repeatedly. Because all three stages of learning occur in a single behavioral session, the paradigm is ideal for the simultaneous observation of the spiking output of multiple single neurons. We use pigeons as model systems, but the task can easily be adapted to any other species capable of conditioned discrimination learning.     

Age-dependent social learning in a lizard

Evidence of social learning, whereby the actions of an animal facilitate the acquisition of new information by another, is taxonomically biased towards mammals, especially primates, and birds. However, social learning need not be limited to group-living animals because species with less interaction can still benefit from learning about potential predators, food sources, rivals and mates. We trained male skinks (Eulamprus quoyii), a mostly solitary lizard from eastern Australia, in a two-step foraging task. Lizards belonging to ‘young’ and ‘old’ age classes were presented with a novel instrumental task (displacing a lid) and an association task (reward under blue lid). We did not find evidence for age-dependent learning of the instrumental task; however, young males in the presence of a demonstrator learnt the association task faster than young males without a demonstrator, whereas old males in both treatments had similar success rates. We present the first evidence of age-dependent social learning in a lizard and suggest that the use of social information for learning may be more widespread than previously believed.     

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus)

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.     

Observational learning in three species of insectivorous bats (Chiroptera)

The potential importance of observational learning has been discussed for many orders of animals, but experimental evidence of this phenomenon in undomesticated mammals other than primates is rate. In this study three species of insectivorus vesperilionid bats (Myotis lucifugus, Eptesicus fuscus and Antrozous pallidus) acquired a novel feeding behaviour through interaction with a knowledgeable conspecific or, in some cases, a bat of another species. The response was not acquired through trial-and-error learning, and conditioning the response took significantly longer than acqisition by observing another bat.     

Life-Long Well Being: Applying Animal Welfare Science to Nonhuman Primates in Sanctuaries

Nonhuman primates have become common in sanctuaries, and a few such facilities even specialize in their care. Sanctuaries can improve the well being of many unwanted primates, especially in terms of housing and socialization. However, diverse facilities call themselves sanctuaries, and they have varying conditions, care programs, and restrictions. In addition, a general lack of regulation of sanctuaries for nonhuman animals creates problems in enforcing even minimal standards. The application of animal welfare science in the sanctuary setting can help foster high standards and empirically based decision making. Sanctuaries offer excellent environments for studying primates without the limitations inherent in breeding, exhibition, and medical research facilities. However, some sanctuaries avoid scientific study. Many sanctuaries have little opportunity to study animal welfare in a systematic manner due to financial considerations or a lack of specific expertise among staff and volunteers. Most published sanctuary research involves reintroduction procedures at sanctuaries in source countries. Nevertheless, one chimpanzee sanctuary's successes in performing long-term studies and using simple evaluation methods, such as check sheets, have demonstrated the benefits of applying animal welfare science to sanctuary-housed nonhuman primates.     

The function and mechanism of vocal accommodation in humans and other primates

The study of non‐human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non‐human primates. An increasing body of research, however, suggests that various species of non‐human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non‐human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception–production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non‐human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre‐adaptations that may have paved the way for language evolution.     

Detecting social learning using networks: a users guide

Controversy over claims of cultures in nonhuman primates and other animals has led to a call for quantitative methods that are able to infer social learning from freely interacting groups of animals. Network-based diffusion analysis (NBDA) is such a method that infers social transmission of a behavioral trait when the pattern of acquisition follows the social network. As, relative to other animals, primates may be unusual in their heavy reliance on social learning, with learning frequently directed along pathways of association; in this study, we draw attention to the significance of this method for primatologists. We provide a "users guide" to NBDA methodology, discussing the choice of NBDA model and social network, and suggest model selection procedures. We also present the results of simulations that suggest that NBDA works well even when the assumptions of the underlying model are violated.     

Do woodpecker finches acquire tool-use by social learning?

Tool-use is widespread among animals, but except in primates the development of this behaviour is poorly known. Here, we report on the first experimental study to our knowledge of the mechanisms underlying the acquisition of tool-use in a bird species. The woodpecker finch Cactospiza pallida, endemic to the Galápagos Islands, is a famous textbook example of tool-use in animals. This species uses modified twigs or cactus spines to pry arthropods out of tree holes. Using nestlings and adult birds from the field, we tested experimentally whether woodpecker finches learn tool-use socially. We show that social learning is not essential for the development of tool-use: all juveniles developed tool-use regardless of whether or not they had a tool-using model. However, we found that not all adult woodpecker finches used tools in our experiments. These non-tool-using individuals also did not learn this task by observing tool-using conspecifics. Our results suggest that tool-use behaviour depends on a very specific learning disposition that involves trial-and-error learning during a sensitive phase early in ontogeny.     

Learning by Observation: Insights from Williams Syndrome

Observing another person performing a complex action accelerates the observer’s acquisition of the same action and limits the time-consuming process of learning by trial and error. Observational learning makes an interesting and potentially important topic in the developmental domain, especially when disorders are considered. The implications of studies aimed at clarifying whether and how this form of learning is spared by pathology are manifold. We focused on a specific population with learning and intellectual disabilities, the individuals with Williams syndrome. The performance of twenty-eight individuals with Williams syndrome was compared with that of mental age- and gender-matched thirty-two typically developing children on tasks of learning of a visuo-motor sequence by observation or by trial and error. Regardless of the learning modality, acquiring the correct sequence involved three main phases: a detection phase, in which participants discovered the correct sequence and learned how to perform the task; an exercise phase, in which they reproduced the sequence until performance was error-free; an automatization phase, in which by repeating the error-free sequence they became accurate and speedy. Participants with Williams syndrome beneficiated of observational training (in which they observed an actor detecting the visuo-motor sequence) in the detection phase, while they performed worse than typically developing children in the exercise and automatization phases. Thus, by exploiting competencies learned by observation, individuals with Williams syndrome detected the visuo-motor sequence, putting into action the appropriate procedural strategies. Conversely, their impaired performances in the exercise phases appeared linked to impaired spatial working memory, while their deficits in automatization phases to deficits in processes increasing efficiency and speed of the response. Overall, observational experience was advantageous for acquiring competencies, since it primed subjects’ interest in the actions to be performed and functioned as a catalyst for executed action.     

Evaluating new technology for biodiversity monitoring: Are drone surveys biased?

Drones and machine learning‐based automated detection methods are being used by ecologists to conduct wildlife surveys with increasing frequency. When traditional survey methods have been evaluated, a range of factors have been found to influence detection probabilities, including individual differences among conspecific animals, which can thus introduce biases into survey counts. There has been no such evaluation of drone‐based surveys using automated detection in a natural setting. This is important to establish since any biases in counts made using these methods will need to be accounted for, to provide accurate data and improve decision‐making for threatened species. In this study, a rare opportunity to survey a ground‐truthed, individually marked population of 48 koalas in their natural habitat allowed for direct comparison of the factors impacting detection probability in both ground observation and drone surveys with manual and automated detection. We found that sex and host tree preferences impacted detection in ground surveys and in manual analysis of drone imagery with female koalas likely to be under‐represented, and koalas higher in taller trees detected less frequently when present. Tree species composition of a forest stand also impacted on detections. In contrast, none of these factors impacted on automated detection. This suggests that the combination of drone‐captured imagery and machine learning does not suffer from the same biases that affect conventional ground surveys. This provides further evidence that drones and machine learning are promising tools for gathering reliable detection data to better inform the management of threatened populations.     

Imitative behavior. A theoretical view

This article reviews the results of experimental studies on imitative behavior reported by various investigators, and then discusses the possible brain mechanisms responsible for this behavior. It was found that human infants in their first hours of life were already capable of spontaneous imitation of simple motor acts demonstrated by an adult, without previous training or reward; these observations suggest that imitative behavior is an innate process that can be considered an unconditional reflex of imitation. It was also found that satiated animals resumed eating when they saw their companions eating. In the latter case, the imitative reflex triggered the previously acquired feeding behavior. Similar mechanisms could be responsible for the phenomenon of eating more in the presence of companions than in their absence, as well as that of preferring the food chosen by companions. When followed by a reward, the imitative act can be learned--that is, transformed into an instrumental conditional response; learning by imitation of simple motor acts was observed in animals, and that of complex motor acts was observed in children who had already achieved a certain developmental stage. In animals, learning complex motor tasks was facilitated by previous observation of a companion performing this task. In this case, the presence of the observer during the session could lead to habituation of the experimental situation and production of associations between this situation and stimuli or emotions related to the reward or punishment, and might result in more efficient learning later. The imitative behavior can be inhibited by stimuli producing responses antagonistic to the act of imitation.     

The behaviour and ecology of wild orang-utans (Pongo pygmaeus)

Between June 1968 and November 1971, 21 months of fieldwork were spent studying wild populations of orang-utans in Borneo and Sumatra. Fifteen hundred hours of daylight observation were made on these animals. In contrast to other higher primates, the dispersed distribution of food and the orang-utan's slow mode of travel seem to favour solitary habits. Over, 80 per cent of foraging units seen contined only one independent animal, either alone or with dependent young. Larger groupings were seen when adolescents joined up with other animals or when males and females formed temporary consortships for mating purposes. Comparison between several populations revealed an interesting mechanisms for the natural regulation of animal numbers. Differences between Bornean and Sumatran orang-utans are discussed in relation to the zoogeography of these two islands.     

Cognitive and affective outcomes of teaching about poisonous and venomous animals

ABSTRACT

The use of live animals in instruction plays an important role in biological education, with the intention that attitudes and emotions should be positively influenced. To date, studies in this field have given mixed results, and there has certainly been a lack of studies on student attitudes and knowledge of poisonous and venomous animals. This study focuses on the effect of the use of poisonous and venomous animals in biology instruction. Two treatment groups of Slovenian seventh and eighth graders (N = 123; age 12.3 and 13.2 years, respectively) were compared. The experimental group (N = 82) was given the opportunity to observe with adequate risk assessment live animal species. The observation of live poisonous and venomous animals led to higher values on different attitudinal dimensions. After instruction, we found no differences between both treatment groups in knowledge. Interest in learning about the different poisonous and venomous animals increased significantly. The level of disgust decreased for the viper, spider, and scorpion. However, ‘fear’ seems to be more stable and less influenceable than ‘disgust’. We recommend that students should be offered as many first-hand experiences with live poisonous and venomous animals as possible mainly through informal learning environments, such as zoos.     

Rhesus Monkeys (Macaca mulatta) Detect Rhythmic Groups in Music,but Not the Beat

It was recently shown that rhythmic entrainment, long considered a human-specific mechanism, can be demonstrated in a selected group of bird species, and, somewhat surprisingly, not in more closely related species such as nonhuman primates. This observation supports the vocal learning hypothesis that suggests rhythmic entrainment to be a by-product of the vocal learning mechanisms that are shared by several bird and mammal species, including humans, but that are only weakly developed, or missing entirely, in nonhuman primates. To test this hypothesis we measured auditory event-related potentials (ERPs) in two rhesus monkeys (Macaca mulatta), probing a well-documented component in humans, the mismatch negativity (MMN) to study rhythmic expectation. We demonstrate for the first time in rhesus monkeys that, in response to infrequent deviants in pitch that were presented in a continuous sound stream using an oddball paradigm, a comparable ERP component can be detected with negative deflections in early latencies (Experiment 1). Subsequently we tested whether rhesus monkeys can detect gaps (omissions at random positions in the sound stream; Experiment 2) and, using more complex stimuli, also the beat (omissions at the first position of a musical unit, i.e. the ‘downbeat’; Experiment 3). In contrast to what has been shown in human adults and newborns (using identical stimuli and experimental paradigm), the results suggest that rhesus monkeys are not able to detect the beat in music. These findings are in support of the hypothesis that beat induction (the cognitive mechanism that supports the perception of a regular pulse from a varying rhythm) is species-specific and absent in nonhuman primates. In addition, the findings support the auditory timing dissociation hypothesis, with rhesus monkeys being sensitive to rhythmic grouping (detecting the start of a rhythmic group), but not to the induced beat (detecting a regularity from a varying rhythm).     

Using deep neural networks to evaluate object vision tasks in rats

In the last two decades rodents have been on the rise as a dominant model for visual neuroscience. This is particularly true for earlier levels of information processing, but a number of studies have suggested that also higher levels of processing such as invariant object recognition occur in rodents. Here we provide a quantitative and comprehensive assessment of this claim by comparing a wide range of rodent behavioral and neural data with convolutional deep neural networks. These networks have been shown to capture hallmark properties of information processing in primates through a succession of convolutional and fully connected layers. We find that performance on rodent object vision tasks can be captured using low to mid-level convolutional layers only, without any convincing evidence for the need of higher layers known to simulate complex object recognition in primates. Our approach also reveals surprising insights on assumptions made before, for example, that the best performing animals would be the ones using the most abstract representations–which we show to likely be incorrect. Our findings suggest a road ahead for further studies aiming at quantifying and establishing the richness of representations underlying information processing in animal models at large.     

Hunted Woolly Monkeys (Lagothrix poeppigii) Show Threat-Sensitive Responses to Human Presence

Responding only to individuals of a predator species which display threatening behaviour allows prey species to minimise energy expenditure and other costs of predator avoidance, such as disruption of feeding. The threat sensitivity hypothesis predicts such behaviour in prey species. If hunted animals are unable to distinguish dangerous humans from non-dangerous humans, human hunting is likely to have a greater effect on prey populations as all human encounters should lead to predator avoidance, increasing stress and creating opportunity costs for exploited populations. We test the threat sensitivity hypothesis in wild Poeppigi''s woolly monkeys (Lagothrix poeppigii) in Yasuní National Park, Ecuador, by presenting human models engaging in one of three behaviours “hunting”, “gathering” or “researching”. These experiments were conducted at two sites with differing hunting pressures. Visibility, movement and vocalisations were recorded and results from two sites showed that groups changed their behaviours after being exposed to humans, and did so in different ways depending on the behaviour of the human model. Results at the site with higher hunting pressure were consistent with predictions based on the threat sensitivity hypothesis. Although results at the site with lower hunting pressure were not consistent with the results at the site with higher hunting pressure, groups at this site also showed differential responses to different human behaviours. These results provide evidence of threat-sensitive predator avoidance in hunted primates, which may allow them to conserve both time and energy when encountering humans which pose no threat.     

Social Network Analysis Shows Direct Evidence for Social Transmission of Tool Use in Wild Chimpanzees

Social network analysis methods have made it possible to test whether novel behaviors in animals spread through individual or social learning. To date, however, social network analysis of wild populations has been limited to static models that cannot precisely reflect the dynamics of learning, for instance, the impact of multiple observations across time. Here, we present a novel dynamic version of network analysis that is capable of capturing temporal aspects of acquisition—that is, how successive observations by an individual influence its acquisition of the novel behavior. We apply this model to studying the spread of two novel tool-use variants, “moss-sponging” and “leaf-sponge re-use,” in the Sonso chimpanzee community of Budongo Forest, Uganda. Chimpanzees are widely considered the most “cultural” of all animal species, with 39 behaviors suspected as socially acquired, most of them in the domain of tool-use. The cultural hypothesis is supported by experimental data from captive chimpanzees and a range of observational data. However, for wild groups, there is still no direct experimental evidence for social learning, nor has there been any direct observation of social diffusion of behavioral innovations. Here, we tested both a static and a dynamic network model and found strong evidence that diffusion patterns of moss-sponging, but not leaf-sponge re-use, were significantly better explained by social than individual learning. The most conservative estimate of social transmission accounted for 85% of observed events, with an estimated 15-fold increase in learning rate for each time a novice observed an informed individual moss-sponging. We conclude that group-specific behavioral variants in wild chimpanzees can be socially learned, adding to the evidence that this prerequisite for culture originated in a common ancestor of great apes and humans, long before the advent of modern humans.     

Risky Business? Lethal Attack by a Jaguar Sheds Light on the Costs of Predator Mobbing for Capuchins (Cebus capucinus)

While some primates attempt to avoid predation by fleeing or hiding, others actually approach, harass, and sometimes attack potential predators, a behavior known as mobbing. Mobbing seems to invite obvious risks, but predators have rarely been observed to injure or kill animals that harass them. The true costs of predator mobbing and the functional significance of this behavior remain poorly understood. Here, we report a fatal attack by a jaguar (Panthera onca) on a mobbing capuchin (Cebus capucinus) that we observed on Barro Colorado Island, Panama. This rare observation illustrates that mobbing predators such as large felids can, indeed, be costly. However, to understand fully the costs of mobbing, the energetic and opportunity costs that primates incur when they harass predators must also be considered.     

Group mating among Norway rats II. The social dynamics of copulation: Competition,cooperation, and mate choice

The social interactions within groups of Norway rats (Rattus norvegicus) had a strong impact on the individual pattern of copulation which, in turn, affects sperm precedence and the probability of implantation in this species. Males alternated uninterrupted ejaculatory series, augmenting each others' copulatory investment. Females took turns mating after receiving an intromission, collectively potentiating the males' copulatory behaviour; increasing the number of oestrous females increased the number of intromissions and ejaculations achieved by each male but did not affect the amount of copulation experienced by each female. These turn-taking patterns within each sex provided the opportunity to change partners and permitted the emergence of different sex-typical patterns of copulation. Furthermore, the dominant male contributed more intromissions and tended to give each female more ejaculations than the subordinates did. Dominant males were also more likely to inhibit the subordinates' sperm transport. Females competed among themselves for the opportunity to mate with a male as he approached ejaculation and were likely to protect more of the dominant male's sperm transport than the subordinate male's.     

Sex differences in political leadership in an egalitarian society

We test the contribution of sex differences in physical formidability, education, and cooperation to the acquisition of political leadership in a small-scale society. Among forager-farmers from the Bolivian Amazon, we find that men are more likely to exercise different forms of political leadership, including verbal influence during community meetings, coordination of community projects, and dispute resolution. We show that these differences in leadership are not due to gender per se but are associated with men's greater number of cooperation partners, greater access to schooling, and greater body size and physical strength. Men's advantage in cooperation partner number is tied to their participation in larger groups and to the opportunity costs of women's intrahousehold labor. We argue these results highlight the mutual influence of sexual selection and the sexual division of labor in shaping how women and men acquire leadership.