Joyful by nature: approaches to investigate the evolution and function of joy in non-human animals.

The nature and evolution of positive emotion is a major question remaining unanswered in science and philosophy. The study of feelings and emotions in humans and animals is dominated by discussion of affective states that have negative valence. Given the clinical and social significance of negative affect, such as depression, it is unsurprising that these emotions have received more attention from scientists. Compared to negative emotions, such as fear that leads to fleeing or avoidance, positive emotions are less likely to result in specific, identifiable, behaviours being expressed by an animal. This makes it particularly challenging to quantify and study positive affect. However, bursts of intense positive emotion (joy) are more likely to be accompanied by externally visible markers, like vocalisations or movement patterns, which make it more amenable to scientific study and more resilient to concerns about anthropomorphism. We define joy as intense, brief, and event-driven (i.e. a response to something), which permits investigation into how animals react to a variety of situations that would provoke joy in humans. This means that behavioural correlates of joy are measurable, either through newly discovered 'laughter' vocalisations, increases in play behaviour, or reactions to cognitive bias tests that can be used across species. There are a range of potential situations that cause joy in humans that have not been studied in other animals, such as whether animals feel joy on sunny days, when they accomplish a difficult feat, or when they are reunited with a familiar companion after a prolonged absence. Observations of species-specific calls and play behaviour can be combined with biometric markers and reactions to ambiguous stimuli in order to enable comparisons of affect between phylogenetically distant taxonomic groups. Identifying positive affect is also important for animal welfare because knowledge of positive emotional states would allow us to monitor animal well-being better. Additionally, measuring if phylogenetically and ecologically distant animals play more, laugh more, or act more optimistically after certain kinds of experiences will also provide insight into the mechanisms underlying the evolution of joy and other positive emotions, and potentially even into the evolution of consciousness.

Improving Integration of Basic Science into Clinical Medicine: Vertical Integration into Clinical Education (VICE) Activity.

The integration of basic science into clinical clerkships continues to be a challenge in medical curricula. We developed an integrated session for 3rd year medical students enrolled in OB-Gyn/Pediatric Block. The session focused on transplacental and perinatal infections, and consisted of a student-driven pedagogy activity in which students were required to explain the basic science principles behind the pathophysiology of the clinical presentations, the work-up, and the treatment of the infections. This approach helps students understand how basic science knowledge informs clinical practice and potential increase clerkship-level students' confidence as it makes them serve as leaders of active learning modules. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s40670-021-01485-7.

The effects of distance on pointing comprehension in shelter dogs.

The Object Choice Task is a methodology that has been increasingly popular for several decades and many strong claims have been made regarding the differential results between species. However, many studies use differing methodologies and individuals with systematically different backgrounds, which makes any comparisons suspect. One of the methodological differences that has been shown to result in differing responses is distance, both between the objects, and between the object and the gesture. Here, we systematically test these differences with a sample of shelter dogs and note the potential mechanisms underlying the results. Dogs were more successful if the objects were further apart (Distal Object) or the point was very close to the object (Proximal Cue). Success in both of these conditions can be most parsimoniously explained by mechanistic strategies, i.e. strategies that do not rely on mental representation or communicative mechanisms. We also note the results of some pilot data suggesting a non-communicative mechanism (body alignment through touch) by which shelter dogs and other animals may successfully respond when the objects and gestures are distant. We argue that the only point type that likely relies on communicative mechanisms is when the objects are close together, but the point is distant the condition in which dogs are least successful. Future research should take into consideration that individual dogs may use different strategies, or may switch between strategies, and note that all point-following is not necessarily indicative of communicative comprehension.

The Question of Capacity: Why Enculturated and Trained Animals have much to Tell Us about the Evolution of Language.

For more than a century researchers have used enculturated animals-those extensively trained or reared by humans-to explore the effects of learning and environment on the capacities for linguistic abilities outside of the human line. Unfortunately, due to many controversies, the findings of these studies frequently have been dismissed or outright ignored. However, experimental exploration of the capacities of nonhumans is the only option to determine which, if any, language-associated capacities are unique to humans. Researchers continue to publish findings from language projects that move our understanding forward, including descriptions of capacities, such as gestural comprehension, declarative communication, and categorization, that are frequently considered to be specific biological adaptations.

Does size really matter? Investigating cognitive differences in spatial memory ability based on size in domestic dogs.

The study of canine cognition can be useful in understanding the selective pressures affecting cognitive abilities. Dogs have undergone intensive artificial selection yielding distinctive breeds, which differ both phenotypically and behaviorally and no other species has a wider range in brain size. As brain size has long been hypothesized to relate to cognitive capacity, this species offers a useful model to further explore this relationship. The influence of physical size on canine cognition has not been thoroughly addressed, despite the fact that large dogs are often perceived to be 'smarter' than small dogs. To date, this preconception has only recently been addressed and supported in one study comparing large and small dogs in a social cognition task, where large dogs outperformed small dogs in a pointing choice task. We assessed large and small dogs using a series of spatial cognition tasks and detected no differences between the two groups. Further research is needed to clarify why our results failed to compliment previous findings. It is possible that differences found in social cognition tasks may not be due to differences in size, rather they may be based on other factors such as methodology, prior training experience, or past experience with humans in general.

Olfactory Enrichment in California Sea Lions (Zalophus californianus): An Effective Tool for Captive Welfare?

In the wild, California sea lions (Zalophus californianus) are exposed to a wide variety of sensory information, which cannot be replicated in captive environments. Therefore, unique procedures are necessary for maintaining physiological and psychological health in nonhuman animals in captivity. The effects of introducing natural scents to captive enclosures have been investigated in a variety of species, yet they have not been examined in marine mammals. This project explored the behavioral effect of scent added to the environment, with the goal of improving the welfare of sea lions in captivity. Two scent types were introduced: (a) natural scents, found in their native environment, and (b) non-natural scents, not found in their native environment. This study examined not only scent enrichment but also the possible evolutionary underpinnings of pinniped olfaction. Scent enrichment was found to significantly impact sea lion behavior as demonstrated by a reduction in pattern swimming, an increase in habitat utilization, and a reduction in stereotypical behavior. However, there were no differences in behavior between natural and non-natural scent conditions.

Gestural and symbolic development among apes and humans: support for a multimodal theory of language evolution.

What are the implications of similarities and differences in the gestural and symbolic development of apes and humans?This focused review uses as a starting point our recent study that provided evidence that gesture supported the symbolic development of a chimpanzee, a bonobo, and a human child reared in language-enriched environments at comparable stages of communicative development. These three species constitute a complete clade, species possessing a common immediate ancestor. Communicative behaviors observed among all species in a clade are likely to have been present in the common ancestor. Similarities in the form and function of many gestures produced by the chimpanzee, bonobo, and human child suggest that shared non-verbal skills may underlie shared symbolic capacities. Indeed, an ontogenetic sequence from gesture to symbol was present across the clade but more pronounced in child than ape. Multimodal expressions of communicative intent (e.g., vocalization plus persistence or eye-contact) were normative for the child, but less common for the apes. These findings suggest that increasing multimodal expression of communicative intent may have supported the emergence of language among the ancestors of humans. Therefore, this focused review includes new studies, since our 2013 article, that support a multimodal theory of language evolution.

Apes communicate about absent and displaced objects: methodology matters.

Displaced reference is the ability to refer to an item that has been moved (displaced) in space and/or time, and has been called one of the true hallmarks of referential communication. Several studies suggest that nonhuman primates have this capability, but a recent experiment concluded that in a specific situation (absent entities), human infants display displaced reference but chimpanzees do not. Here, we show that chimpanzees and bonobos of diverse rearing histories are capable of displaced reference to absent and displaced objects. It is likely that some of the conflicting findings from animal cognition studies are due to relatively minor methodological differences, but are compounded by interpretation errors. Comparative studies are of great importance in elucidating the evolution of human cognition; however, greater care must be taken with methodology and interpretation for these studies to accurately reflect species differences.

The role of socio-communicative rearing environments in the development of social and physical cognition in apes.

The cultural intelligence hypothesis (CIH) claims that humans' advanced cognition is a direct result of human culture and that children are uniquely specialized to absorb and utilize this cultural experience (Tomasello, 2000). Comparative data demonstrating that 2.5-year-old human children outperform apes on measures of social cognition but not on measures of physical cognition support this claim (Herrmann et al., 2007). However, the previous study failed to control for rearing when comparing these two species. Specifically, the human children were raised in a human culture whereas the apes were raised in standard sanctuary settings. To further explore the CIH, here we compared the performance on multiple measures of social and physical cognition in a group of standard reared apes raised in conditions typical of zoo and biomedical laboratory settings to that of apes reared in an enculturated socio-communicatively rich environment. Overall, the enculturated apes significantly outperformed their standard reared counterparts on the cognitive tasks and this was particularly true for measures of communication. Furthermore, the performance of the enculturated apes was very similar to previously reported data from 2.5-year-old children. We conclude that apes who are reared in a human-like socio-communicatively rich environment develop superior communicative abilities compared to apes reared in standard laboratory settings, which supports some assumptions of the cultural intelligence hypothesis.

Nonhuman Primates do Declare! A Comparison of Declarative Symbol and Gesture Use in Two Children, Two Bonobos, and A Chimpanzee.

While numerous publications have shown that apes can learn some aspects of human language, one frequently cited difference between humans and apes is the relative infrequency of declaratives (comments and statements) as opposed to imperatives (requests) in ape symbol use. This paper describes the use of declaratives in three language-competent apes and two children. The apes produced a lower proportion of spontaneous declaratives than did the children. However, both groups used declaratives to name objects, to interact and negotiate, and to make comments about other individuals. Both apes and children also made comments about past and future events. However, showing/offering/giving, attention getting, and comments on possession were declarative types made by the children but rarely by the apes.

Planum temporale grey matter asymmetries in chimpanzees (Pan troglodytes), vervet (Chlorocebus aethiops sabaeus), rhesus (Macaca mulatta) and bonnet (Macaca radiata) monkeys.

Brain asymmetries, particularly asymmetries within regions associated with language, have been suggested as a key difference between humans and our nearest ancestors. These regions include the planum temporale (PT) - the bank of tissue that lies posterior to Heschl's gyrus and encompasses Wernicke's area, an important brain region involved in language and speech in the human brain. In the human brain, both the surface area and the grey matter volume of the PT are larger in the left compared to right hemisphere, particularly among right-handed individuals. Here we compared the grey matter volume and asymmetry of the PT in chimpanzees and three other species of nonhuman primate in two Genera including vervet monkeys (Chlorocebus aethiops sabaeus), rhesus macaques (Macaca mulatta) and bonnet macaques (Macaca radiata). We show that the three monkey species do not show population-level asymmetries in this region whereas the chimpanzees do, suggesting that the evolutionary brain development that gave rise to PT asymmetry occurred after our split with the monkey species, but before our split with the chimpanzees.

The impact of environment on the comprehension of declarative communication in apes.

A series of recent reports have questioned the ability of great apes to comprehend declarative communication and have suggested that this ability is biologically based and may have driven the evolution of human language. We tested three groups of differently reared chimpanzees and bonobos for their ability to understand declarative signals in an object-choice task. The scores of the two groups of apes that were reared in a sociolinguistically complex environment were significantly higher than the scores of the standard-reared group. The results further showed that bonobos did not outperform chimpanzees. Our results demonstrate that environmental factors, particularly access to a sociolinguistically rich environment, directly influence great apes' ability to comprehend declarative signals and suggest that, contrary to recent claims, apes have the biological capacity to utilize purely informative communication.

The influence of feeding, enrichment, and seasonal context on the behavior of Pacific Walruses (Odobenus rosmarus divergens).

Though some research exists concerning general behavior and activity patterns of Walruses in zoos or aquariums, less is known about how these patterns change in response to various environmental and temporal contexts. This study presents two studies assessing behavioral changes in relation to feeding period, object enrichment (OE), and season in a social group of four Pacific Walruses at the New York Aquarium. Study 1 examined behavior in relation to feeding context (nonfeed, prefeed, postfeed); data were collected over a three-week period, resulting in 47 observation sessions for each feeding context. Study 2 examined behavior in relation to OE and season; data were collected in two phases resulting in 12 enrichment and 9 no-enrichment (NE) observation sessions (Phase 1), and 21 enrichment and 18 NE observation sessions (Phase 2). Study 1 showed that after feeding, oral behavior increased while social behavior and total swim frequency decreased. In Study 2, both swim frequency and social behavior were found to interact with OE and phase, while oral behavior remained constant across all conditions. As in the wild, both studies found all animals to be swimming the majority of the time. Though every animal spent much of its swim time engaged in an Individual Swimming Pattern (ISP), both studies showed that the proportion of ISP (in relation to total time swimming) remained stable across all contexts, suggesting a potential functional role of the ISPs. These results are discussed in light of the ongoing debate over the role of stereotypies in welfare assessment.

Volumetric and lateralized differences in selected brain regions of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus).

The two species of Pan, bonobos and common chimpanzees, have been reported to have different social organization, cognitive and linguistic abilities and motor skill, despite their close biological relationship. Here, we examined whether bonobos and chimpanzee differ in selected brain regions that may map to these different social and cognitive abilities. Eight chimpanzees and eight bonobos matched on age, sex and rearing experiences were magnetic resonance images scanned and volumetric measures were obtained for the whole brain, cerebellum, striatum, motor-hand area, hippocampus, inferior frontal gyrus and planum temporale. Chimpanzees had significantly larger cerebellum and borderline significantly larger hippocampus and putamen, after adjusting for brain size, compared with bonobos. Bonobos showed greater leftward asymmetries in the striatum and motor-hand area compared with chimpanzees. No significant differences in either the volume or lateralization for the so-called language homologs were found between species. The results suggest that the two species of Pan are quite similar neurologically, though some volumetric and lateralized differences may reflect inherent differences in social organization, cognition and motor skills.

Mental representation of symbols as revealed by vocabulary errors in two bonobos (Pan paniscus).

Error analysis has been used in humans to detect implicit representations and categories in language use. The present study utilizes the same technique to report on mental representations and categories in symbol use from two bonobos (Pan paniscus). These bonobos have been shown in published reports to comprehend English at the level of a two-and-a-half year old child and to use a keyboard with over 200 visuographic symbols (lexigrams). In this study, vocabulary test errors from over 10 years of data revealed auditory, visual, and spatio-temporal generalizations (errors were more likely items that looked like sounded like, or were frequently associated with the sample item in space or in time), as well as hierarchical and conceptual categorizations. These error data, like those of humans, are a result of spontaneous responding rather than specific training and do not solely depend upon the sample mode (e.g. auditory similarity errors are not universally more frequent with an English sample, nor were visual similarity errors universally more frequent with a photograph sample). However, unlike humans, these bonobos do not make errors based on syntactical confusions (e.g. confusing semantically unrelated nouns), suggesting that they may not separate syntactical and semantic information. These data suggest that apes spontaneously create a complex, hierarchical, web of representations when exposed to a symbol system.