Antonella Tramacere

This chapter offers a brief review of theories on mirror neuron development, highlighting different models. These models focus on either the role of genetic mechanisms or the contributions of experience and of learning processes in shaping the brain circuits involved in action–perception coupling. As an alternative, the chapter proposes an epigenetic model for mirror neuron development, explaining how such a model can help to elucidate, within a unifying explanatory framework, the emergence, diversity, and functional reuse of mirror neurons. Lastly, a related evolutionary scenario is sketched in which epigenetic regulation, genetic assimilation/the Baldwin effect, and niche construction play crucial roles in mirror neuron evolution.

In the current opinion paper, we provide a comparative perspective on specific aspects of primate empathic abilities, with particular emphasis on the mirror neuron system associated with mouth/face actions and expression. Mouth and faces can be very salient communicative classes of stimuli that allow an observer access to the emotional and physiological content of other individuals. We thus describe patterns of activations of neural populations related to observation and execution of specific mouth actions and emotional facial expressions in some species of monkeys and in humans. Particular attention is given to dynamics of face-to-face interactions in the early phases of development and to the differences in the anatomy of facial muscles among different species of primates. We hypothesize that increased complexity in social environments and patterns of social development have promoted specializations of facial musculature, behavioral repertoires related to production and recognition of facial emotional expression, and their neural correlates. In several primates, mirror circuits involving parietal-frontal regions, insular regions, cingulate cortices, and amygdala seem to support automatic forms of embodied empathy, which probably contribute to facial mimicry and behavioural synchrony. In humans these circuits interact with specific prefrontal and temporo-parietal cortical regions, which facilitates higher order cognitive functions such as cognitive empathy and mental state attribution. Our analysis thus suggests that the evolution of higher forms of empathy, such as mentalizing, is also linked to the coupling between the perceptual and motor system related to face processing, which may have undergone a process of exaptation during primate phylogeny.

Considering the properties of mirror neurons (MNs) in terms of development and phylogeny, we offer a novel, unifying, and testable account of their evolution according to the available data and try to unify apparently discordant research, including the plasticity of MNs during development, their adaptive value and their phylogenetic relationships and continuity. We hypothesize that the MN system reflects a set of interrelated traits, each with an independent natural history due to unique selective pressures, and propose that there are at least three evolutionarily significant trends that gave raise to three subtypes: hand visuomotor, mouth visuomotor, and audio–vocal. Specifically, we put forward a mosaic evolution hypothesis, which posits that different types of MNs may have evolved at different rates within and among species. This evolutionary hypothesis represents an alternative to both adaptationist and associative models. Finally, the review offers a strong heuristic potential in predicting the circumstances under which specific variations and properties of MNs are expected. Such predictive value is critical to test new hypotheses about MN activity and its plastic changes, depending on the species, the neuroanatomical substrates, and the ecological niche.

Songbirds possess mirror neurons (MNs) activating during the perception and execution of specific features of songs. These neurons are located in high vocal center (HVC), a premotor nucleus implicated in song perception, production and learning, making worth to inquire their properties and functions in vocal recognition and imitative learning. By integrating a body of brain and behavioral data, we discuss neurophysiology, anatomical, computational properties and possible functions of songbird MNs. We state that the neurophysiological properties of songbird MNs depends on sensorimotor regions that are outside the auditory neural system. Interestingly, songbirds MNs can be the result of the specific type of song representation possessed by some songbird species. At the functional level, we discuss whether songbird MNs are involved in others' song recognition, by dissecting the function of recognition in various different but possible overlapping processes: action-oriented perception, discriminative-oriented perception and identification of the signaler. We conclude that songbird MNs may be involved in recognizing other singer's vocalizations, while their role in imitative learning still require to solve how auditory feedback are used to correct own vocal performance to match the tutor song. Finally, we compare songbird and human mirror responses, hypothesizing a case of convergent evolution, and proposing new experimental directions.

Humans are uncontroversially better than other species at learning from their peers. A key example of this is imitation, the ability to reproduce both the means and ends of others’ behaviours. Imitation is critical to the acquisition of a number of uniquely human cultural and cognitive traits. However, while authors largely agree on the importance of imitation, they disagree about the origins of imitation in humans. Some argue that imitation is an adaptation, connected to the ‘Mirror Neuron System’ that evolved to facilitate action understanding and the learning of social behaviours. Others argue that imitation is a cultural practice learned in childhood, and that there is no evidence that it evolved genetically. We offer a third alternative that is consistent with both data that the human brain is optimised for imitation, and consistent with its being substantially learned. We hypothesise that at some point in human history humans underwent natural selection for two imitation-relevant abilities – specifically, (i) the tendency to be more attentive to our peers, and (ii) fine motor skill in the manual and oro-facial domains. These changes enabled us to excel at both learning to imitate, and learning by imitating.

In this paper, we distinguish between a number of different phenomena that have been called imitation, and identify one form—a high fidelity mechanism for social learning—considered to be crucial for the development of language. Subsequently, we consider a common claim in the language evolution literature, which is that prior to the emergence of vocal language our ancestors communicated using a sophisticated gestural protolanguage, the learning of some parts of which required manual imitation. Drawing upon evidence from recent work in neuroscience, primatology, and archeology, we argue that while gestural communication undoubtedly played a crucial role in language evolution, the grounds for thinking that manual imitation did are currently unconvincing.