Raising an Eye at Facial Muscle Morphology in Canids.

The evolution of facial muscles in dogs has been linked to human preferential selection of dogs whose faces appear to communicate information and emotion. Dogs who convey, especially with their eyes, a sense of perceived helplessness can elicit a caregiving response from humans. However, the facial muscles used to generate such expressions may not be uniquely present in all dogs, but rather specifically cultivated among various taxa and individuals. In a preliminary, qualitative gross anatomical evaluation of 10 canid specimens of various species, we find that the presence of two facial muscles previously implicated in human-directed canine communication, the levator anguli occuli medialis (LAOM) and the retractor anguli occuli lateralis (RAOL), was not unique to domesticated dogs (Canis familiaris). Our results suggest that these aspects of facial musculature do not necessarily reflect selection via human domestication and breeding. In addition to quantitatively evaluating more and other members of the Canidae family, future directions should include analyses of the impact of superficial facial features on canine communication and interspecies communication between dogs and humans.

Are there dedicated neural mechanisms for imitation? A study of grist and mills.

Are there brain regions that are specialized for the execution of imitative actions? We compared two hypotheses of imitation: the mirror neuron system (MNS) hypothesis predicts frontal and parietal engagement which is specific to imitation, while the Grist-Mills hypothesis predicts no difference in brain activation between imitative and matched non-imitative actions. Our delayed imitation fMRI paradigm included two tasks, one where correct performance was defined by a spatial rule and another where it was defined by an item-based rule. For each task, participants could learn a sequence from a video of a human hand performing the task, from a matched "Ghost" condition, or from text instructions. When participants executed actions after seeing the Hand demonstration (compared to Ghost and Text demonstrations), no activation differences occurred in frontal or parietal regions; rather, activation was localized primarily to occipital cortex. This adds to a growing body of evidence which indicates that imitation-specific responses during action execution do not occur in canonical mirror regions, contradicting the mirror neuron system hypothesis. However, activation differences did occur between action execution in the Hand and Ghost conditions outside MNS regions, which runs counter to the Grist-Mills hypothesis. We conclude that researchers should look beyond these hypotheses as well as classical MNS regions to describe the ways in which imitative actions are implemented by the brain.

What Is Written on a Dog's Face? Evaluating the Impact of Facial Phenotypes on Communication between Humans and Canines.

Facial phenotypes are significant in communication with conspecifics among social primates. Less is understood about the impact of such markers in heterospecific encounters. Through behavioral and physical phenotype analyses of domesticated dogs living in human households, this study aims to evaluate the potential impact of superficial facial markings on dogs' production of human-directed facial expressions. That is, this study explores how facial markings, such as eyebrows, patches, and widow's peaks, are related to expressivity toward humans. We used the Dog Facial Action Coding System (DogFACS) as an objective measure of expressivity, and we developed an original schematic for a standardized coding of facial patterns and coloration on a sample of more than 100 male and female dogs (N = 103), aged from 6 months to 12 years, representing eight breed groups. The present study found a statistically significant, though weak, correlation between expression rate and facial complexity, with dogs with plainer faces tending to be more expressive (r = -0.326, p ≤ 0.001). Interestingly, for adult dogs, human companions characterized dogs' rates of facial expressivity with more accuracy for dogs with plainer faces. Especially relevant to interspecies communication and cooperation, within-subject analyses revealed that dogs' muscle movements were distributed more evenly across their facial regions in a highly social test condition compared to conditions in which they received ambiguous cues from their owners. On the whole, this study provides an original evaluation of how facial features may impact communication in human-dog interactions.

Generative cultural learning in children and adults: the role of compositionality and generativity in cultural evolution.

Are human cultures distinctively cumulative because they are uniquely compositional? We addressed this question using a summative learning paradigm where participants saw different models build different tower elements, consisting of discrete actions and objects: stacking cubes (tower base) and linking squares (tower apex). These elements could be combined to form a tower that was optimal in terms of height and structural soundness. In addition to measuring copying fidelity, we explored whether children and adults (i) extended the knowledge demonstrated to additional tower elements and (ii) productively combined them. Results showed that children and adults copied observed demonstrations and applied them to novel exemplars. However, only adults in the imitation condition combined the two newly derived base and apex, relative to adults in a control group. Nonetheless, there were remarkable similarities between children's and adults' performance across measures. Composite measures capturing errors and overall generativity in children's and adults' performance produced few population by condition interactions. Results suggest that early in development, humans possess a suite of cognitive skills-compositionality and generativity-that transforms phylogenetically widespread social learning competencies into something that may be unique to our species, cultural learning; allowing human cultures to evolve towards greater complexity.

Applying computational modeling to assess age-, sex-, and strategy-related differences in Spin the Pots, a working memory task for 2- to 4-year-olds.

Working memory (WM) develops rapidly during early childhood. In the present study, visual WM (VSM) was measured using the well-established Spin the Pots task (Hughes & Ensor, 2005), a complex non-verbal eight-location object occlusion task. A self-ordered hiding procedure was adopted to allow for an examination of children's strategy use during a VWM task. Participants (N = 640) between the ages of 2 and 4 years were tested under semi-naturalistic conditions, in the home or in a museum. Computational modeling was used to estimate an expected value for the total trials to complete Spin the Pots via a random search and child performance was compared to expected values. Based on this approach, we determined that children who found six stickers retrieved them in significantly fewer trials than the expected value, excluding chance performance and implicating VWM. Results also showed age-related and sex-related changes in VWM. Between 2 and 4 years of age, 4-year-olds performed significantly better than younger children and girls out-performed the boys. Spontaneous use of a color matching hiding strategy was associated with a higher success rate on the task. Implications of these findings for early development of VWM are discussed.

Optimizing imitation: Examining cognitive factors leading to imitation, overimitation, and goal emulation in preschoolers.

Humans imitate patently irrelevant actions known as overimitation, and rather than decreasing with age, overimitation increases with age. Whereas most overimitation research has focused on social factors associated with overimitation, comparatively little is known about the cognitive- and task-specific features that influence overimitation. Specifically, developmental contrasts between imitation and overimitation are confounded by the addition of irrelevant actions to causally necessary actions, increasing sequence length, cognitive load, and processing costs-variables known to be age dependent. We constructed a novel puzzle box task such that a four-step imitation, four-step overimitation, and two-step efficient sequence could be demonstrated using the same apparatus on video. In Experiments 1 and 2, 2.5- to 5-year-olds randomly assigned to imitation and overimitation groups performed significantly more target actions than baseline control groups. Rates of imitation and overimitation increased as a function of age, with older preschoolers outperforming younger preschoolers in both conditions. In Experiment 3, preschoolers were shown a video of an efficient two-step demonstration prior to testing. After they responded, they were shown a four-step overimitation video and were tested on the same puzzle box. Children imitated the efficient demonstration, but after watching the overimitation video, they also overimitated the irrelevant actions. Once again, older children overimitated more than younger children. Together, results show that preschoolers are faithful, flexible, and persistent overimitators. The fidelity and flexibility of overimitation are constrained not only by social factors but also by basic cognitive processes that vary across age groups. As these constraints diminish, overimitation and flexible (optimal) imitation increases.

Intuitive invention by summative imitation in children and adults.

Humanity's ability to conquer every corner of the planet rests on our inventiveness. But is this inventiveness best explained by individual problem-solving skills or by our species' exceptional social learning abilities? Using a tower-building task, we show that, on average, 3% of 4-6 year old children (n = 180) and adults (n = 192) independently combined tower pieces to produce the most optimal tower possible, confirming that preschool age children and adults alike are poor independent inventors. Yet, after observing one or more models generate tower elements separately, both children and adults reproduced the demonstrated elements and spontaneously combined them, producing a novel (unobserved) tower of optimal height, evidence of intuitive invention by summative imitation. These results challenge folk concepts of innovation and corroborate those from mathematical models showing that our species' inventiveness generally arise from social learning rather than individual insights. So, rather than being sui generis, human inventions are, broadly, communis generis.

Specialization in the vicarious learning of novel arbitrary sequences in humans but not orangutans.

Sequence learning underlies many uniquely human behaviours, from complex tool use to language and ritual. To understand whether this fundamental cognitive feature is uniquely derived in humans requires a comparative approach. We propose that the vicarious (but not individual) learning of novel arbitrary sequences represents a human cognitive specialization. To test this hypothesis, we compared the abilities of human children aged 3-5 years and orangutans to learn different types of arbitrary sequences (item-based and spatial-based). Sequences could be learned individually (by trial and error) or vicariously from a human (social) demonstrator or a computer (ghost control). We found that both children and orangutans recalled both types of sequence following trial-and-error learning; older children also learned both types of sequence following social and ghost demonstrations. Orangutans' success individually learning arbitrary sequences shows that their failure to do so in some vicarious learning conditions is not owing to general representational problems. These results provide new insights into some of the most persistent discontinuities observed between humans and other great apes in terms of complex tool use, language and ritual, all of which involve the cultural learning of novel arbitrary sequences. This article is part of the theme issue 'Ritual renaissance: new insights into the most human of behaviours'.

Only domain-specific imitation practice makes imitation perfect.

Does imitation involve specialized mechanisms or general-unspecialized-learning processes? To address this question, preschoolers (3- and 4-year-olds) were assigned to one of four "practice" groups. Before and after the practice phases, each group was tested on a novel Spatial Imitation sequence. During the practice phase, children in the Spatial Imitation group practiced jointly attending, vicariously encoding, and copying the novel spatial sequences. In the Item Imitation group, children practiced jointly attending, vicariously encoding, and copying novel item sequences. In the Trial-and-Error group, children practiced encoding and recalling a series of novel spatial sequences entirely through individual (operant) learning. In the Free Play (no practice) control group, children played a touchscreen drawing game that controlled for practice time on the touchscreen and mirrored some of the same actions and responses used in the experimental conditions. Results of the difference between pre- and post-practice effects on novel spatial imitation sequences showed that only the Spatial Imitation practice group significantly improved relative to the Free Play group. Individual Spatial Trial-and-Error practice did not significantly improve spatial imitation. The effect of Item Imitation practice was intermediate. These results are inconsistent with the hypothesis that general processes alone--or primarily--support imitation learning and is more consistent with a mosaic model that posits an additive-interaction-effect on imitation performance where a more general social cognitive mechanism (i.e., natural pedagogy) gathers the relevant information from the demonstration and another more specialized mechanism (i.e., imitation specific) transforms that information into a matching response.

Neural responses when learning spatial and object sequencing tasks via imitation.

Humans often learn new things via imitation. Here we draw on studies of imitation in children to characterise the brain system(s) involved in the imitation of different sequence types using functional magnetic resonance imaging. On each trial, healthy adult participants learned one of two rule types governing the sequencing of three pictures: a motor-spatial rule (in the spatial task) or an object-based rule (in the cognitive task). Sequences were learned via one of three demonstration types: a video of a hand selecting items in the sequence using a joystick (Hand condition), a computer display highlighting each item in order (Ghost condition), or a text-based demonstration of the sequence (Text condition). Participants then used a joystick to execute the learned sequence. Patterns of activation during demonstration observation suggest specialisation for object-based imitation in inferior frontal gyrus, specialisation for spatial sequences in anterior intraparietal sulcus (IPS), and a general preference for imitation in middle IPS. Adult behavioural performance contrasted with that of children in previous studies-indicating that they experienced more difficulty with the cognitive task-while neuroimaging results support the engagement of different neural regions when solving these tasks. Further study is needed on whether children's differential performance is related to delayed IPS maturation.

Re-examination of Oostenbroek et al. (2016): evidence for neonatal imitation of tongue protrusion.

The meaning, mechanism, and function of imitation in early infancy have been actively discussed since Meltzoff and Moore's (1977) report of facial and manual imitation by human neonates. Oostenbroek et al. (2016) claim to challenge the existence of early imitation and to counter all interpretations so far offered. Such claims, if true, would have implications for theories of social-cognitive development. Here we identify 11 flaws in Oostenbroek et al.'s experimental design that biased the results toward null effects. We requested and obtained the authors' raw data. Contrary to the authors' conclusions, new analyses reveal significant tongue-protrusion imitation at all four ages tested (1, 3, 6, and 9 weeks old). We explain how the authors missed this pattern and offer five recommendations for designing future experiments. Infant imitation raises fundamental issues about action representation, social learning, and brain-behavior relations. The debate about the origins and development of imitation reflects its importance to theories of developmental science.

Animal studies help clarify misunderstandings about neonatal imitation.

Empirical studies are incompatible with the proposal that neonatal imitation is arousal driven or declining with age. Nonhuman primate studies reveal a functioning brain mirror system from birth, developmental continuity in imitation and later sociability, and the malleability of neonatal imitation, shaped by the early environment. A narrow focus on arousal effects and reflexes may grossly underestimate neonatal capacities.

What's Special about Human Imitation? A Comparison with Enculturated Apes.

What, if anything, is special about human imitation? An evaluation of enculturated apes' imitation skills, a "best case scenario" of non-human apes' imitation performance, reveals important similarities and differences between this special population of apes and human children. Candidates for shared imitation mechanisms include the ability to imitate various familiar transitive responses and object-object actions that involve familiar tools. Candidates for uniquely derived imitation mechanisms include: imitating novel transitive actions and novel tool-using responses as well as imitating opaque or intransitive gestures, regardless of familiarity. While the evidence demonstrates that enculturated apes outperform non-enculturated apes and perform more like human children, all apes, regardless of rearing history, generally excel at imitating familiar, over-rehearsed responses and are poor, relative to human children, at imitating novel, opaque or intransitive responses. Given the similarities between the sensory and motor systems of preschool age human children and non-human apes, it is unlikely that differences in sensory input and/or motor-output alone explain the observed discontinuities in imitation performance. The special rearing history of enculturated apes-including imitation-specific training-further diminishes arguments suggesting that differences are experience-dependent. Here, it is argued that such differences are best explained by distinct, specialized mechanisms that have evolved for copying rules and responses in particular content domains. Uniquely derived social and imitation learning mechanisms may represent adaptations for learning novel communicative gestures and complex tool-use. Given our species' dependence on both language and tools, mechanisms that accelerated learning in these domains are likely to have faced intense selective pressures, starting with the earliest of human ancestors.

Vocal overimitation in preschool-age children.

Overimitation--copying incorrect, idiosyncratic, or causally irrelevant actions--has been linked to our species' long history with artifacts whose functions are often opaque. It is an open question, however, whether children overimitate outside the artifact domain. We explored this question by presenting preschool-age children (3- to 5-year-olds, N=120) with an elicited imitation task that included high- and low-frequency disyllabic nouns (e.g., 'pizza) and nonwords (e.g., 'chizza), all of which had a stressed first syllable. However, during testing, half of the stimuli were incorrectly pronounced by stressing the second syllable (e.g., pi'zza). More than half of the children copied the model's incorrect pronunciation of high-frequency familiar words, consistent with overimitation. This pattern of response persisted even after children had themselves correctly named the familiar words prior to the start of testing, confirming that children purposefully altered the pronunciation of known words to match the incorrect pronunciations used by a model. These results demonstrate that overimitation is not restricted to the artifact domain and might extend to many different tasks and domains.

Children with autism spectrum disorder have an exceptional explanatory drive.

An "explanatory drive" motivates children to explain ambiguity. Individuals with autism spectrum disorders are interested in how systems work, but it is unknown whether they have an explanatory drive. We presented children with and without autism spectrum disorder unsolvable problems in a physical and in a social context and evaluated problem-solving and explanation-seeking responses. In the physical context (but not the social context), the children with autism spectrum disorder showed a stronger explanatory drive than controls. Importantly, the number of explanatory behaviors made by children with autism spectrum disorder in the social context was independent of social and communicative impairments. Children with autism spectrum disorder did not show an exceptional explanatory drive in the social domain. These results suggest that children with autism spectrum disorder have an explanatory drive and that the explanatory drive may be domain specific.

The cognitive structure of goal emulation during the preschool years.

Humans excel at mirroring both others' actions (imitation) as well as others' goals and intentions (emulation). As most research has focused on imitation, here we focus on how social and asocial learning predict the development of goal emulation. We tested 215 preschool children on two social conditions (imitation, emulation) and two asocial conditions (trial-and-error and recall) using two touch screen tasks. The tasks involved responding to either three different pictures in a specific picture order (Cognitive: apple→boy→cat) or three identical pictures in a specific spatial order (Motor-Spatial: up→down→right). Generalized linear models demonstrated that during the preschool years, Motor-Spatial emulation is associated with social and asocial learning, while cognitive emulation is associated only with social learning, including motor-spatial emulation and multiple forms of imitation. This result contrasts with those from a previous study using this same data set showing that motor-spatial and cognitive imitation were neither associated with one another nor, generally, predicted by other forms of social or asocial learning. Together, these results suggests that while developmental changes in imitation are associated with multiple - specialized - mechanisms, developmental changes in emulation are associated with age-related changes and a more unitary, domain-general mechanism that receives input from several different cognitive and learning processes, including some that may not necessarily be specialized for social learning.

Sequential recall of meaningful and arbitrary sequences by orangutans and human children: Does content matter?

Do visual cues such as size, color, and number facilitate sequential recall in orangutans and human children? In Experiment 1, children and adult orangutans solved two types of sequences, arbitrary (unrelated pictures) and meaningful (pictures varied along a spectrum according to the size, color, or number of items shown), in a touchscreen paradigm. It was found that visual cues did not increase the percentage of correct responses for either children or orangutans. In order to demonstrate that the failure to spontaneously seriate along these dimensions was not due to a general inability to perceive the dimensions nor to an inability to seriate items, in Experiment 2, orangutans were trained on one type of sequence and tested on novel sequences organized according to the same rule (i.e., pictures varied on the number spectrum only). The orangutans performed significantly better on novel meaningful sequences in this task than on novel arbitrary sequences. These results indicate that, while orangutans and human children share the ability to learn how to order items according to their size, color, or number, both orangutans and humans lack a cognitive propensity to spontaneously (i.e., without prior training or enculturation) order multiple items by size, color, or number.