The Neurobiology of Cultural Intelligence Mosaic of Mirror Neurons. The Neurobiology of Cultural Intelligence Antonella Tramacere Lichtenberg-Kolleg/The Göttingen Institute for Advanced Study  &  The German Primate Center/Leibniz Institute for Primate Research  Georg-August-Universität Göttingen The evolution of cultural intelligence The distinctive aspects of primate cognition evolved mainly in response to the challenging demands of a complex social life constituted by constant competition and cooperation in social groups (social intelligence hypothesis). If primates are social, humans are “ultra-social”. Indeed, whereas primates have evolved social-cognitive skills for competing and cooperating with conspecifics, humans have also evolved skills (i.e., specialized social learning, language and “theory of mind”) that enable them to create different cultural groups (cultural intelligence hypothesis) (Hermann et al. 2007). The social intelligence hypothesis is supported by positive correlations between relative brain size (i.e., neocortex) and social variables, such as group or grooming clique size, as index of social complexity (Dunbar 2003). However, this only provides generic support for the cultural intelligence hypothesis. Overall correlations do not explicate the brain size differences in relation to social cognitive skills, nor do they help us to identify which neural substrates humans deploy during specific cognitive tasks that others primates do not. Neural correlates of social cognition Assuming that mirror neurons (MNs) are an important feature of the social brain (by underlying the capacity of the individual to transform social sensorial information into a motor format), I test whether MNs properties and variations across different primate species confirm the prediction of the cultural intelligence hypothesis. Accordingly, I propose a parsimonious categorization that may help to clarify the properties of MNs by taking into account two unambiguous physiological criteria: the modalities of sensory input triggering the response, and the effectors involved in the motor output. I obtained three main categories: hand (visuomotor) MNs, mouth (visuomotor) MNs and audio-vocal MNs (Tramacere et al. 2016). Mouth Mirror Neurons Mouth MNs (indirectly investigated in humans and macaques) activate during the observation and execution of same or similar actions performed with the mouth. Mouth MNs are likely present from birth, and associated with phenomena of early facial communication in the context of mother – infant interactions. They seem to be a common heritage of anthropoid primates, which have evolved early facial responsiveness and visual attraction to others faces. Elettrophysiological investigations in lemurs, which are supposed to lack these features in the neonatal phase of development, could be instrumental to confirm this hypothesis (Tramacere & Ferrari 2016). A B C Fig. 1. A) Macaque newborn showing attention and responsiveness to others’ mouth actions during lab experimental condition. B) Macaque mother-infant facial exchange. C) Lemur mother carrying infants on the back. Hand Mirror Neurons Hand MNs (directly investigated in marmoset and macaque, and indirectly in chimpanzee and human) activate during observation and execution of manual actions, in correspondent cerebral areas (dorsal stream). However, only in humans hands MNs strongly activate during mimicking actions (Rizzolatti and Sinigaglia 2010 ). In contrast, monkey hand MNs are very weakly sensitive to non-goal directed movements (Nelissen et al. 2011 ), while in chimpanzee these neurons activate more than in the monkey, but significantly less strongly than in humans. Further, in macaques there is a large discrepancy between the ventral and the dorsal streams (circuits associated with respectively the coding of the end-result of observed actions, and with the spatial coding of movements and finer level of action kinematics). This difference is less pronounced in chimpanzees and absent in humans (Hecht et al. 2012 ). Fig. 2. Hand mirror neurons (MNs) in humans, chimpanzees and macaques. Specific anatomical regions of human (A), chimpanzee (B) and macaque (C) brains activated during observation of grasping overlap with regions activated during the execution of the same grasping action. Premotor, parietal and sensory areas are shown in green, red and yellow, respectively. The blue arrow represent the dorsal stream. (PM) premotor cortex, (IFG) inferior frontal gyrus, (IPL) inferior parietal lobule, (M1) primary motor cortex, (SMA) supplementary motor area, (STS) superior temporal sulcus, cytoarchitectonic areas BA44 (known as Broca’s area), BA45 and BA6, PF, PFG, FCBm, F5. Audio-Vocal Mirror Neurons Audio-vocal MNs activate during both listening and execution of specific vocal cues. They seem to be associated with auditory feedback and vocal learning (Mooney 2014) in songbirds and in human beings, where they have been investigated respectively directly and indirectly. Whereas humans and songbirds convergently evolved audio-vocal MNs, non-human primates lack the neural substrates for vocal learning. Indeed, while the emergence of a rudimentary auditory-motor control in monkey brains under conditional learning shares many features with the neural pathways of auditory-vocal integration that has been observed in expert vocal learners, monkey vocal conditioning seems to not be associated with any audio-vocal MNs (Coude´ et al. 2011 )—suggesting that it relies on different mechanisms from human speech. Fig. 3. Songbirds and humans, both vocal learners, have a similar pattern in the way premotor/motor areas are connected to the brainstem in the establishment of learned vocalizations. Both non-songbirds and macaques (which lack these patterns) can be trained to vocalize voluntarily and consequently to establish connections between the premotor cortex and motoneurons. However, no evidences exist in relation to the possibility to develop audio-vocal MNs in premotor or regions of the brain. (RA) robust nucleus of the arcopallium, (XII) motoneurons of the syrinx, (HVC) high vocal centre, (Area X) striatal nucleus, (DLM) dorsolateral nucleus of the medial thalamus, (LMC) face area of the primary motor cortex, (Am) nucleus ambiguous, (Ast) anterior striatum, (At) anterior thalamus (PAG), periacqueductal grey area, (ACC) anterior cingulate cortex. A role for Mirror Neurons in the Cultural Intelligence Hypothesis The comparative analysis of various sub-types of MNs can be a useful tool for identifying potential mechanisms underlying the evolution of social cognition, and testing the predictions of the cultural intelligence hypothesis. Specifically, considering MNs as a mosaic of distinct although interrelated traits can be instrumental to identify evolutionary changes that occur in some brain parts, without simultaneous changes in other parts. Mechanisms of neural mirroring seem to be evolved in different primate species with different timing and precursors, with a relatively independent evolutionary history and in relation to different social and environmental demands. Further, humans seem to be endowed with more sophisticated and multiple mirroring mechanisms. Indeed, if mouth MNs may not be implicated in unique humans social capacities, hand and audio-vocal MNs seem to associated with action-processes oriented social and vocal learning (Tramacere and Moore 2016).