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Published in final edited form as: Interact Stud. 2018 Sep 17;19(1-2):38–53.

Reflections on the differential organization of mirror neuron systems for hand and mouth and their role in the evolution of communication in primates

Gino Coudé 1, Pier Francesco Ferrari 1
PMCID: PMC8916705  NIHMSID: NIHMS1037165  PMID: 35283699

Abstract

It is now generally accepted that the motor system is not purely dedicated to the control of behavior, but also has cognitive functions. Mirror neurons have provided a new perspective on how sensory information regarding others’ actions and gestures is coupled with the internal cortical motor representation of them. This coupling allows an individual to enrich his interpretation of the social world through the activation of his own motor representations. Such mechanisms have been highly preserved in evolution as they are present in humans, apes and monkeys. Recent neuroanatomical data showed that there are two different connectivity patterns in mirror neuron networks in the macaque: one is concerned with sensorimotor transformation in relation to reaching and hand grasping within the traditional parietal-premotor circuits; the second one is linked to the mouth/face motor control and the new data show that it is connected with limbic structures. The mouth mirror sector seems to be wired not only for ingestive behaviors but also for orofacial communicative gestures and vocalizations. Notably, the hand and mouth mirror networks partially overlap, suggesting the importance of hand-mouth synergies not only for sensorimotor transformation, but also for communicative purposes in order to better convey and control social signals.

INTRODUCTION

The motor system has always been referred to as a complex network evolved to control behavior. Although this view is still partly true, it has been challenged by the discovery of mirror neurons (MNs) in macaques (di Pellegrino et al., 1992; Gallese et al., 1996). MNs, in fact, provide a motor template through which the perception of others’ behavior activates in the observer the same motor representations used during the execution of the behavior. Due to this additional property, our understanding of the motor system has expanded its role from a purely controlling machine to a system heavily involved in social cognition. The striking properties of MNs led also to the hypothesis that they might be involved in some aspects of language or communication (Rizzolatti and Arbib, 1998).

In the present review, we first briefly describe the neuroanatomical connections of the mirror system, complementing the well-charted understanding of the manual mirror system by emphasizing that its relatively overlooked component: the mouth mirror system, has a dramatically different pattern of connectivity with other brain regions, bringing in the limbic system. Secondly, we describe neuroethological studies that link the mouth sector of the premotor cortex to facial mimicry and vocalization. Finally, we speculate that in primates, hand and mouth motor synergies have been at the core of complex forms of communication.

MIRRORING OTHERS’ ACTIONS AND GESTURES THROUGH THE MOTOR SYSTEM

One of the most striking features of the motor system is its involvement in decoding others’ behavior through a mechanism in which the sensory (either visual or acoustic) description of an action is translated into a motor format. By exploiting the rich neuroanatomical network sustaining sensorimotor transformations at the service of pragmatic functions (i.e. reaching and grasping an object), the motor system has expanded its functions within a social domain. The discovery of MNs represents therefore an important landmark in our comprehension of the mechanisms and functions of the motor system because it has provided a new perspective on how sensory information regarding others’ actions/gestures is coupled with the internal cortical motor representation of it. This coupling allows the creation of a matching mechanism enabling individuals to enrich their interpretation of the social world through the activation their own motor representations that have been built in the course of phylogeny and ontogeny.

Hand and mouth: two different mirror networks

MNs discharge when a subject either actually performs a motor act or simply observes the same act being performed by someone else. In other words, the observation of an action triggers in the observer’s brain a representation of that action in a motor format (Rizzolatti and Sinigaglia, 2016). One of the key features of MNs is that of generalizing the visual stimulus that triggers the neuron response from self’s action to others’ action (Tramacere et al., 2016; Maranesi et al., 2017).The likely starting process through which this generalization process emerged is embedded in the properties of the motor system which in the course of the arm movement is capable of visually tracking one’s own hand to reach the target (Oztop and Arbib, 2002; Maranesi et al., 2017) Such visuo-motor coupling, necessary for grasping objects, has been exploited during evolution in order to track others’ grasping actions.

The literature about MNs is abundant and the connectivity pattern of hand-related mirror neurons has been amply described elsewhere (see Rizzolatti et al., 2014; Borra et al., 2017), therefore, we will not further review it here beyond presenting the top half of Figure 1. In this section, we will instead emphasize the anatomical connections of the mouth mirror sector that lies in the lateral sector of F5c (lateral to the hand sector with an overlapping hand-mouth area) and in the bordering dorsal opercular (DO) cortex.

Figure 1.

Figure 1.

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Summary of the hand and the mouth mirror neuron networks. The connectivity of the hand mirror neuron network is based on the description of neural tracer injections placed in the dorsal part of area F5 in which the hand mirror neurons were found. Specifically, the connections indicated are based on those observed in previous works. The connectivity of the mouth mirror neuron network is based on the description of neural tracer injections placed in the ventral part of area F5 and in the opercular areas GrFO and DO in which the mouth mirror. Adapted from Ferrari et al. (2017).

Mouth MNs form a category of neurons that mirror ingestive and communicative mouth actions. In fact, a small percentage of mouth MNs respond to communicative gestures such as lip-smacking, a typical macaque affiliative gesture (Ferrari et al., 2003). Recent neuroanatomical data (Ferrari et al., 2017) have shown that the connectivity pattern of the cortical sector of mouth MNs is different from the one subserving hand MNs. We thus proposed that the mirror mechanism is composed and supported by, at least, two different anatomical pathways (Figure 1). As mentioned above, one of these pathways is concerned with sensorimotor transformation in relation to reaching and hand grasping within the traditional parietal-premotor circuits. The other is linked to mouth/face motor control and is connected with limbic structures, involved in facial expression and processing of emotions as well as processing of reward. Note that there is a significant overlap between the hand and mouth representations within the ventral PMv.

Processing reward and social context

Unlike the hand regions, the mouth mirror sector has strong connections with the anterior cingulate cortex, orbitofrontal cortex, the anterior insula, and the basolateral amygdala. The projections to the anterior cingulate cortex are likely targeting a region involved in emotional processing of information in relation to reward value or to the relevance of behaviors linked to outcomes (Hayden et al., 2010; Cai and Padoa-Schioppa, 2012). Interestingly, neuroimaging studies showed that the observation and imitation of facial expressions of emotions activates a region of the anterior cingulate cortex (Carr et al., 2003; Singer et al., 2004). The link of the mouth mirror sector with the anterior cingulate cortex could be therefore important to process information regarding food value for programming and selecting ingestive activities. It can also be exploited within the social communication domain since there is a link between ACC and the basic affiliative and communicative behaviors (see Apps et al., 2016), as well as with cost-benefit decisions made within social context (Hillman and Bilkey, 2012). The mouth mirror sector is also connected with the orbitofrontal cortex, known to be involved in coding reward value obtained in social context (Azzi et al., 2012). These connections show that the mouth mirror system has access to information related to ingestion and food rewards as well as of social nature.

Mouth mirror access to visual information does not occur via the parietal cortex

The hand mirror sector has been shown to have direct anatomical connections to parietal regions AIP and PFG (Rozzi et al., 2006; Gerbella et al., 2011). It has been proposed that these parietal areas transmit visual information regarding hand grasping movement and constitute a hub for the visual input coming from the superior temporal sulcus (STS) (Nelissen and Vanduffel, 2011). However, the mouth mirror sector is connected with parietal areas (Bruni et al., 2017) mostly related to somatosensory and motor representations of the face and of the mouth. We can hypothesize that the visual information serving orofacial or communicative behaviors comes through pathways involving the ventral prefrontal cortex areas (12 and 46), the insula and the amygdala. The ventrolateral prefrontal cortex is connected with mouth mirror sector (Ferrari et al., 2017), and with the temporal sectors that are contributing to the coding of biological motion and facial expressions, and to the processing of complex stimuli linked to vocalizations (Barbas, 1988; Romanski, 2012; Gerbella et al., 2013). It is also possible that the information related to facial expressions and/or its emotional content could reach the mouth mirror sector via its connections with the orbitofrontal cortex, the insula or the amygdala.

Facial gestural communication and the face mirror network

The mouth mirror sector sends projections to the facial nucleus for the innervation of the lower part of the face, likely involved in motor control of the mimic facial muscles (Morecraft et al., 2001), a group of muscles in the region of the face that make the physical expression of emotions possible through their movements. As mentioned above, the mouth sector has strong connections with limbic structures known to be involved in encoding emotional facial expressions and processing reward and motivation: the anterior cingulate cortex, the anterior and mid-dorsal insula, the orbitofrontal cortex and the basolateral amygdala. This connectivity pattern is probably reflected in the fact that mouth mirror neurons fire during intransitive (communicative) actions in monkeys, while hand mirror neurons do not. Interestingly, the mid-dorsal insula is a structure known to provoke affiliative facial expression when electrically stimulated (Caruana et al., 2011; Jezzini et al., 2012). The mouth sector also has connections with the ventral sector of the putamen, a region that is part of a circuit related to motivated behavior and that is involved in foraging behavior (Tremblay et al., 2015). These anatomical data are in agreement with neurophysiological evidence showing that in the mouth MNs F5/opercular region there are neurons responding to facial communicative gestures (e.g. lipsmacking) (Ferrari et al., 2017).

From a functional perspective, it is possible that the lateral sector of the F5/opercular region has a motor control on the facial mimic muscles for communicative purposes. The capacity to activate motor programs corresponding with those observed may suggest that a mirror mechanism could underpin some behavioral phenomena that require a prompt and matched response to a communicative signal sent by a conspecific. Such mimicry phenomena have been documented in nonhuman primates and they are highly relevant in affiliative context where individuals coordinate face-to-face exchanges, either during play behaviors or during mother-infant affective communication (Ferrari et al., 2006; Mancini et al., 2013).

Facial mimicry (see example in Figure 2) is a common behavioral phenomenon that consists in a form of affective dyadic exchange in which the affective state of one individual facilitates the activation of a similar motor program in the receiver. It also activates the bodily/autonomic responses that are associated to it. Other forms of emotional contagion (Hatfield et al., 1993) have been described in animals (emotion recognition, emotion contagion, and emotion priming), even though the neural mechanisms responsible for them are still unknown (Decety and Jackson, 2006; Singer, 2006; Lamm et al., 2011; Walter, 2011). Although these forms of emotional contagion are common and their very basic response probably do not require complex cognitive processes, they may nevertheless constitute the building block of rudimentary forms of empathy. In fact, many scholars believe that MNs, or at least a mirroring mechanism, can account for some rudimentary forms of empathy, like facial mimicry (Preston and Waal, 2002; de Vignemont and Singer, 2006). Mouth MNs and the mirroring of facial mimicry are probably at the basis of the capacity to become emotionally attuned with another individual.

Figure 2.

Figure 2.

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Example of facial mimicry during play in two Gelada Baboons (Photo by Pier Francesco Ferrari).

According to Preston and de Waal (2002) empathy is in fact a multilayer phenomenon which has at its core some mechanisms coupling action and perception. Empathy can thus be defined as the ability to understand and share the internal states of others. Several scholars agree that it is a complex, multidimensional phenomenon that includes a number of functional processes, including emotion recognition, emotion contagion, and emotion priming (see Decety and Lamm, 2006), as well as the abilities to react to the internal states of others, and to distinguish between one’s own and others’ internal states (see Tomova et al., 2014). Empathy can take various forms along a spectrum. At one end of this spectrum, mimicry and emotional contagion appear to be shared by several mammalian species, like primates, mice, pigs and dogs (see Tramacere and Ferrari, 2016). At the other end of this spectrum, higher forms of empathy such as cognitive empathy rely on a conscious, deliberative process through which inferences can be made about others’ bodily and affective states, beliefs, and intentions - often referred to as “mentalizing” - (Keysers and Fadiga, 2008; Zaki and Ochsner, 2012).

Hand mouth synergies

There is a significant overlap between the hand and mouth representations within the ventral PMv (Maranesi et al., 2012). Neurons discharging for mouth, hand actions or gestures are often intermingled. Such motor organization, with overlapping hand and mouth motor representations, has been previously described (McGuinness et al., 1980; Huang et al., 1988). Interestingly, electrically evoked complex movements have been also reported in the monkey (Graziano et al., 2002; Kaas et al., 2013), and they often involve coordinated movements of the hand and of the mouth. These ethologically relevant movements seem to reflect synergistic responses aimed at optimizing behaviors that are relevant for survival. The somatotopic and functional organization of the motor cortex facilitates the recruitment of the cortical motor commands involved in the control of facial muscles when the combined movements of hand and mouth are requested (Graziano et al., 2005; Desmurget et al., 2014).

The use of the hand in affecting mouth responses is also supported by numerous human kinematic studies by Gentilucci and colleagues showing that the movement of the hand during grasping affects the simultaneous kinematics of the mouth during different motor tasks. Another series of investigations showed that the grasping of objects of different size influences the motor command for mouth opening (Gentilucci and Campione, 2011).

Hand and mouth integration could also be achieved through thalamic relays. Thalamic projections to the mouth mirror sector derive from the anterior nuclei associated with sensory-motor functions (VA; X), but also from more posterior nuclei such as MD. This nucleus is also connected with the prefrontal areas 46v and 12, which contain neurons responsive during the execution of hand and mouth actions (Simone et al., 2015) and during action observation (Simone et al., 2017). Areas 46v and 12 are, in turn, linked with the mouth mirror sector. This trans-thalamic interplay could modulate the efficacy of direct inputs from one cortical area to another (Sherman, 2007; Saalmann and Kastner, 2011). It could likely reflect the integration of hand and mouth motor synergies in coordinated motor sequences that are required during foraging behaviors. This suggests that some aspects of the motor control of the hand and of the mouth are neurophysiologically coordinated in order to support synergies during hand-mouth interaction, when the monkey grasps food and brings it to the mouth, for instance (Gentilucci et al., 1988; Ferrari et al., 2003).

Hand mouth synergies for gestural communication

The link between the hand and the mouth has been hypothesized to be integrated also within the communication domain. Several gestures in primates can involve the oro-facial or/and the brachiomanual system in conjunction with body postures. Facial gestures often involve face-to-face exchanges, involuntary acts and autonomic responses (Ferrari et al., 2006). Some of these gestures have been extensively studied by comparative investigations that could reconstruct, with reliable approximation, their possible relatedness and origin among the different species (van Hooff, 1967).

Regarding brachio-manual gestural communication, apes use them in a richer and more elaborated way than monkeys (Call and Tomasello, 2007). In the last ten years there has been an increasing body of research, in part stimulated by the idea that brachio-manual gestures have probably played a role in language evolution (Arbib et al., 2008; Liebal and Call, 2012). Apes, for example, are able to use several types of gestures, often in combination, to request food (Leavens et al., 2004, 2005; Gómez, 2007). In captivity, chimpanzees and also some monkeys point to request food or objects and, in the case of chimpanzees, they are sensitive to the attentional state of the human experimenter when they point (Leavens et al., 2004b). Although they do not gesture to share information or to inform others, it has been pointed out that they might use brachio-manual gestures in many flexible ways. Under human rearing conditions some apes have been reported to use declarative gestures, thus showing the potential to expand their cognitive and contextual use of the communicative gesture (Lyn et al., 2011). There are several lines of converging evidence from neuroscience, ethology and developmental psychology that many of the gestures displayed by nonhuman primates began their existence as actions devoid of a communicative function (Halina et al., 2013; Arbib et al., 2014). Over time, gestures became co-opted and transformed into communicative devices that accomplished similar functions (Fogassi and Ferrari, 2012; Liebal and Call, 2012). Interestingly, a recent brain imaging study in deaf signers found that the Broca’s area, part of the human MN system, is activated during both the observation and execution of hand sign language (Okada et al., 2016). This and other data seem to converge in indicating that a MN system for speech and hand gesture exploits a common brain network (Gentilucci and Corballis, 2006) in which the coupling of sensory and motor information is instrumental to facilitate an efficient signal exchange between the signaler and the recipient.

We propose that MNs followed two different evolutionary trends: hand guidance in space and gestural or vocal communication. However, hand-mouth synergies must have been exploited at a communicative level for better conveying and controlling the transmitted information (Gentilucci and Corballis, 2006). This kind of transition can be seen at a behavioral level in apes, but the corresponding neurophysiological data is missing. Vocalization might have had a late beginning in the evolution, but some of its rudiments are present in extant monkeys.

Towards a New Road Map

Neuroanatomical and ethological data indicate that the motor system is not purely dedicated to the control of behavior, but also plays a role in cognitive functions that are especially relevant in social context, complementing systems “beyond the mirror.” The mirror network neuroanatomical data are also relevant at an evolutionary level. The mirror system hypothesis (MSH) has been elaborated in its core elements on the available knowledge at the time on the main properties of hand mirror neurons and on the related hand mirror circuits (i.e. AIP-PFG-F5). It traces an evolutionary path of the role of mirror neurons within larger systems “beyond the mirror” to provide a path via increasingly complex imitation and pantomime to protosign, with even simple protosign providing support for the emergence of protospeech. Systems beyond the mirror evolve to provide meaning that complements the control and perception of articulation.

The mirror neuron system itself evolved. In this paper, we reviewed its connectivity and posit that there were at least two mirror networks in LCA-m. The fact that more than one mirror neuron network exists in LCA-m might indicate that they were shaped through different evolutionary pathways (with important overlap though), each with an independent natural history due to unique selective pressures. Unlike the hand MN sector, the mouth MN sector, have a set of connections with brain regions that are part of the limbic system and that are involved in emotion and reward processing. This suggests that the mirror neuron circuitry changed or perhaps underwent coordinated evolutionary modifications with neural systems “beyond the mirror”, such as the limbic system. Increasing social complexity favored individuals that are attuned with the emotional states of their peers, especially in species, like monkeys and apes, where parental care is particularly long and is foundational for the emotional and cognitive development of the infant. We can speculate that a mouth MN network with an access to the limbic system has important implications regarding the evolutionary processes that linked emotional communication with facial gestures.

A second important aspect to be considered is how vocalizations could have been integrated in such complex communication system. For long, monkeys’ vocalizations have been considered outside the volitional control and therefore investigated as a system independent from other forms of communication both in terms of mechanical/anatomical and neural control.

The discovery in the PMv of neurons that are activated during conditioned vocalization (Coudé et al., 2011) challenged this view. First, it indicates that volitional control of vocalization might have emerged in anatomical areas overlapping with cortical regions involved in hand and mouth motor control. Whether such anatomical convergence of different effectors had an impact on the potential synergies between vocal control and gestures remains an intriguing hypothesis worth to be investigated. Second, it suggests a timescale for the emergence of vocal control such that some evolutionary pressure must have come into play well before the use of protosigns (i.e. communication based on conventionalized manual gestures) developed. This does not mean that the capability of monkeys to control vocalization “promote“ voice as being a direct route to language. In our view, the vocalization control circuitry in the monkey (LCA-m) was a building block for what would later become the controlled utterances of protospeech. This means that a circuit at least partly dedicated to voluntary vocal control, and emerging from early evolutionary pressures, had opened a restricted path for more complex forms of vocalization. This restricted path, taking advantage of some features of the PMv – among which the overlapping cortical representation of hand, mouth and larynx, and the presence of motor and mirror neurons coding goals independently of the effector used – has probably contributed to make vocal signals “suitable” for further evolutionary changes, where protosign mechanisms are scaffolding protospeech. When writing about the evolutionary expanding spiral involving protosign and protospeech where “mechanisms evolved to support one become available to support the other”, Arbib (2016) writes: “the mechanisms that evolved to support protosign extended collaterals to yield the control of the vocal apparatus that supported an increasingly precise control of vocalization needed to support speech” (see also Arbib’s interesting suggestion on how this vocal control could have evolved, this issue). The neurophysiological and behavioral monkey/ape data, allow to hypothesize that the passage from protosign to protospeech was possible only because the cortical circuitry had, a long time ago (in LCA-m), started a process of shaping vocal control. This process would eventually make vocal control amenable to be scaffolded by protosign and later become protospeech.

Acknowledgements

This research was supported in part by the Division of Intramural Research, NICHD, and NIH P01 HD064653. The paper was prepared for a workshop funded by NSF Grant No. BCS-1343544 “INSPIRE Track 1: Action, Vision and Language, and their Brain Mechanisms in Evolutionary Relationship,” (M.A. Arbib, Principal Investigator).” .

This paper is dedicated to the memory of Maurizio Gentilucci, an outstanding and rigorous scientist, who greatly contributed to our understanding of the mouth-hand motor synergies and their implications for gestural communication.

Biographies

Bibliographical note

Gino Coudé has studied Neuroscience and worked on the neurophysiology of the motor and mirror neurons of the premotor cortex.

Pier Francesco Ferrari has studied Ethology and Neuroscience, investigating the role of premotor and parietal cortex in primate social cognition. His research has also been focused on the brain and social development of both humans and monkeys. He is currently director of research at the Institut des Sciences Cognitives of CNRS in France.

References

  1. Apps MAJ, Rushworth MFS, Chang SWC (2016) The Anterior Cingulate Gyrus and Social Cognition: Tracking the Motivation of Others. Neuron 90:692–707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arbib MA (2016) Towards a Computational Comparative Neuroprimatology: Framing the language-ready brain. Phys Life Rev 16:1–54. [DOI] [PubMed] [Google Scholar]
  3. Arbib MA, Liebal K, Pika S (2008) Primate Vocalization, Gesture, and the Evolution of Human Language. Curr Anthropol 49:1053–1076. [DOI] [PubMed] [Google Scholar]
  4. Arbib M, Ganesh V, Gasser B (2014) Dyadic brain modelling, mirror systems and the ontogenetic ritualization of ape gesture. Philos Trans R Soc B Biol Sci 369:20130414–20130414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Azzi JCB, Sirigu a., Duhamel J-R (2012) Modulation of value representation by social context in the primate orbitofrontal cortex. Proc Natl Acad Sci 109:2126–2131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313–342. [DOI] [PubMed] [Google Scholar]
  7. Borra AE, Gerbella M, Rozzi S, Luppino G (2017) The macaque lateral grasping network: a neural substrate for generating purposeful hand actions. Neurosci Biobehav Rev 75:65–90. [DOI] [PubMed] [Google Scholar]
  8. Bruni S, Gerbella M, Bonini L, Borra E, Coudé G, Francesco P, Fogassi L, Maranesi M, Rodà F, Simone L, Ugolotti F, Rozzi S (2017) Cortical and subcortical connections of parietal and premotor nodes of the monkey hand mirror neuron network. [DOI] [PubMed] [Google Scholar]
  9. Cai X, Padoa-Schioppa C (2012) Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex. J Neurosci 32:3791–3808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Call J, Tomasello M (2007) The gestural communication of apes and monkeys. (Erlbaum L, ed). Mahwah, NJ. [Google Scholar]
  11. Carr L, Iacoboni M, Dubeau M-C, Mazziotta JC, Lenzi GL (2003) Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci U S A 100:5497–5502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Caruana F, Jezzini A, Sbriscia-Fioretti B, Rizzolatti G, Gallese V (2011) Emotional and social behaviors elicited by electrical stimulation of the insula in the macaque monkey. Curr Biol 21:195–199. [DOI] [PubMed] [Google Scholar]
  13. Coudé G, Ferrari PF, Rodà F, Maranesi M, Borelli E, Veroni V, Monti F, Rozzi S, Fogassi L (2011) Neurons controlling voluntary vocalization in the macaque ventral premotor cortex. PLoS One 6:1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. de Vignemont F, Singer T (2006) The empathic brain: how, when and why? Trends Cogn Sci 10:435–441. [DOI] [PubMed] [Google Scholar]
  15. Decety J, Jackson PL (2006) A Social-Neuroscience Perspective on Empathy. Curr Dir Psychol Sci 15:54–58. [Google Scholar]
  16. Decety J, Lamm C (2006) Human Empathy Through the Lens of Social Neuroscience. Sci World J 6:1146–1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Desmurget M, Richard N, Harquel S, Baraduc P, Szathmari A, Mottolese C, Sirigu A (2014) Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus. Proc Natl Acad Sci U S A 111:5718–5722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp brain Res 91:176–180. [DOI] [PubMed] [Google Scholar]
  19. Ferrari PF, Gallese V, Rizzolatti G, Fogassi L (2003) Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur J Neurosci 17:1703–1714. [DOI] [PubMed] [Google Scholar]
  20. Ferrari PF, Visalberghi E, Paukner A, Fogassi L, Ruggiero A, Suomi S (2006) Neonatal Imitation in Rhesus Macaques. PLoS Biol 4:e302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ferrari PFF, Gerbella M, Coudé G, Rozzi S (2017) Two different mirror neuron networks: the sensorimotor (hand) and limbic (face) pathways. Neuroscience 358:300–315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fogassi L, Ferrari P (2012) Cortical Motor Organization, Mirror Neurons, and Embodied Language: An Evolutionary Perspective. Biolinguistics:308–337. [Google Scholar]
  23. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119 ( Pt 2:593–609. [DOI] [PubMed] [Google Scholar]
  24. Gentilucci M, Campione GC (2011) Do postures of distal effectors affect the control of actions of other distal effectors? evidence for a system of interactions between hand and mouth. PLoS One 6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gentilucci M, Corballis MC (2006) From manual gesture to speech: a gradual transition. Neurosci Biobehav Rev 30:949–960. [DOI] [PubMed] [Google Scholar]
  26. Gentilucci M, Fogassi L, Luppino G, Matelli M, Camarda R, Rizzolatti G (1988) Functional organization of inferior area 6 in the macaque monkey - I. Somatotopy and the control of proximal movements. Exp Brain Res 71:475–490. [DOI] [PubMed] [Google Scholar]
  27. Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2011) Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5. Brain Struct Funct 216:43–65. [DOI] [PubMed] [Google Scholar]
  28. Gerbella M, Borra E, Tonelli S, Rozzi S, Luppino G (2013) Connectional heterogeneity of the ventral part of the macaque area 46. Cereb Cortex 23:967–987. [DOI] [PubMed] [Google Scholar]
  29. Gómez JC (2007) Pointing behaviors in apes and human infants: A balanced interpretation. Child Dev 78:729–734. [DOI] [PubMed] [Google Scholar]
  30. Graziano MSA, Aflalo TNS, Cooke DF (2005) Arm movements evoked by electrical stimulation in the motor cortex of monkeys. J Neurophysiol 94:4209–4223. [DOI] [PubMed] [Google Scholar]
  31. Graziano MSA, Taylor CSR, Moore T (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841–851. [DOI] [PubMed] [Google Scholar]
  32. Halina M, Rossano F, Tomasello M (2013) The ontogenetic ritualization of bonobo gestures. Anim Cogn 16:653–666. [DOI] [PubMed] [Google Scholar]
  33. Hatfield E, Cacioppo J, Rapson R (1993) Emotional Contagion. Curr Dir Psychol Sci 2:96–99. [Google Scholar]
  34. Hayden BY, Smith DV, Platt ML (2010) Cognitive control signals in posterior cingulate cortex. Front Hum Neurosci 4:223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hillman KL, Bilkey DK (2012) Neural encoding of competitive effort in the anterior cingulate cortex. Nat Neurosci 15:1290–1297. [DOI] [PubMed] [Google Scholar]
  36. Huang CS, Sirisko MA, Hiraba H, Murray GM, Sessle BJ (1988) Organization of the primate face motor cortex as revealed by intracortical microstimulation and electrophysiological identification of afferent inputs and corticobulbar projections. J Neurophysiol 59:796–818. [DOI] [PubMed] [Google Scholar]
  37. Jezzini A, Caruana F, Stoianov I, Gallese V, Rizzolatti G (2012) Functional organization of the insula and inner perisylvian regions. Proc Natl Acad Sci U S A 109:10077–10082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kaas JH, Gharbawie OA, Stepniewska I (2013) Cortical networks for ethologically relevant behaviors in primates. Am J Primatol 75:407–414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Keysers C, Fadiga L (2008) The mirror neuron system: new frontiers. Soc Neurosci 3:193–198. [DOI] [PubMed] [Google Scholar]
  40. Lamm C, Decety J, Singer T (2011) Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage 54:2492–2502. [DOI] [PubMed] [Google Scholar]
  41. Leavens a, Bard a, Sussex E, Kingdom U (2005) Understanding Chimpanzee Epig ? nesis the Pointing and Ecological Validity Point of. Curr Dir Psychol Sci 14:185–189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Leavens D a, Hopkins WD, Thomas RK (2004a) Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 118:48–57. [DOI] [PubMed] [Google Scholar]
  43. Leavens DA, Russell JL, Hopkins WD (2004b) Intentionality as Measured in the Persistence and Elaboration of Communication by Chimpanzees (Pan troglodytes). Child Dev 76:291–306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Liebal K, Call J (2012) The origins of non-human primates’ manual gestures. Philos Trans R Soc B Biol Sci 367:118–128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Lyn H, Greenfield PM, Savage-Rumbaugh S, Gillespie-Lynch K, Hopkins WD (2011) Nonhuman primates do declare! A comparison of declarative symbol and gesture use in two children, two bonobos, and a chimpanzee. Lang Commun 31:63–74. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Mancini G, Ferrari PF, Palagi E (2013) In Play We Trust. Rapid Facial Mimicry Predicts the Duration of Playful Interactions in Geladas. PLoS One 8:2–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Maranesi M, Livi A, Bonini L (2017) Spatial and viewpoint selectivity for others ‘ observed actions in monkey ventral premotor mirror neurons. Sci Rep:1–19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Maranesi M, Rodà F, Bonini L, Rozzi S, Ferrari PF, Fogassi L, Coudé G (2012) Anatomo-functional organization of the ventral primary motor and premotor cortex in the macaque monkey. Eur J Neurosci 36:3376–3387. [DOI] [PubMed] [Google Scholar]
  49. McGuinness E, Sivertsen D, Allman JM (1980) Organization of the face representation in macaque motor cortex. J Comp Neurol 193:591–608. [DOI] [PubMed] [Google Scholar]
  50. Morecraft RJ, Louie JL, Herrick JL, Stilwell-Morecraft KS (2001) Cortical innervation of the facial nucleus in the non-human primate: A new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression. Brain 124:176–208. [DOI] [PubMed] [Google Scholar]
  51. Nelissen K, Vanduffel W (2011) Grasping-related functional magnetic resonance imaging brain responses in the macaque monkey. J Neurosci 31:8220–8229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Okada K, Rogalsky C, O’Grady L, Hanaumi L, Bellugi U, Corina D, Hickok G (2016) An fMRI study of perception and action in deaf signers. Neuropsychologia 82:179–188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Oztop E, Arbib MA (2002) Schema design and implementation of the grasp-related mirror neuron system. Biol Cybern 87:116–140. [DOI] [PubMed] [Google Scholar]
  54. Preston SD, & Waal F. B. M. De. (2002). Empathy: Its ultimate and proximate bases. Behavioral and Brain Sciences, 25(1), 1–71. [DOI] [PubMed] [Google Scholar]
  55. Rizzolatti G, Arbib MA (1998) Language within our grasp. Trends Neurosci 21:188–195. [DOI] [PubMed] [Google Scholar]
  56. Rizzolatti G, Cattaneo L, Fabbri-Destro M, Rozzi S (2014) Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiol Rev 94:655–706. [DOI] [PubMed] [Google Scholar]
  57. Rizzolatti G, Sinigaglia C (2016) The mirror mechanism: a basic principle of brain function. Nat Rev Neurosci 17:757–765. [DOI] [PubMed] [Google Scholar]
  58. Romanski LM (2012) Integration of faces and vocalizations in ventral prefrontal cortex: implications for the evolution of audiovisual speech. Proc Natl Acad Sci U S A 109 Suppl:10717–10724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG, Matelli M, Luppino G (2006) Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 16:1389–1417. [DOI] [PubMed] [Google Scholar]
  60. Saalmann YB, Kastner S (2011) Cognitive and Perceptual Functions of the Visual Thalamus. Neuron 71:209–223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sherman SM (2007) The thalamus is more than just a relay. Curr Opin Neurobiol 17:417–422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Simone L, Bimbi M, Rodà F, Fogassi L, Rozzi S (2017) Action observation activates neurons of the monkey ventrolateral prefrontal cortex. Sci Rep 7:44378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Simone L, Rozzi S, Bimbi M, Fogassi L (2015) Movement-related activity during goal-directed hand actions in the monkey ventrolateral prefrontal cortex. Eur J Neurosci 42:2882–2894. [DOI] [PubMed] [Google Scholar]
  64. Singer T (2006) The neuronal basis and ontogeny of empathy and mind reading: Review of literature and implications for future research. Neurosci Biobehav Rev 30:855–863. [DOI] [PubMed] [Google Scholar]
  65. Singer T, Seymour B, O’Dohery J, Kaube H, Dolan RJ, Frith CD (2004) Empathy for pain involves the affective but not sensory components of pain. Science (80- ) 303:1157–1162. [DOI] [PubMed] [Google Scholar]
  66. Tomova L, Von Dawans B, Heinrichs M, Silani G, Lamm C (2014) Is stress affecting our ability to tune into others? Evidence for gender differences in the effects of stress on self-other distinction. Psychoneuroendocrinology 43:95–104. [DOI] [PubMed] [Google Scholar]
  67. Tramacere A, Ferrari PF (2016) Faces in the mirror, from the neuroscience of mimicry to the emergence of mentalizing. J Anthropol Sci 94:113–126. [DOI] [PubMed] [Google Scholar]
  68. Tramacere A, Pievani T, Ferrari PF (2016) Mirror neurons in the tree of life: mosaic evolution, plasticity and exaptation of sensorimotor matching responses. Biol Rev:0–0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tremblay L, Worbe Y, Thobois S, Sgambato-Faure V, Féger J (2015) Selective dysfunction of basal ganglia subterritories: From movement to behavioral disorders. Mov Disord 30:1155–1170. [DOI] [PubMed] [Google Scholar]
  70. van Hooff JRRAM (1967) The facial displays of catarrhine monkeys and apes. In: Primate Ethology, Weidenfeld. (Morris D, ed), pp 7–68. London. [Google Scholar]
  71. Walter H (2011) Social Cognitive Neuroscience of Empathy – Concepts, circuits and genes. Neuroscience in press:9–17. [Google Scholar]
  72. Zaki J, Ochsner KN (2012) The neuroscience of empathy: progress, pitfalls and promise. Nat Neurosci 15:675–680. [DOI] [PubMed] [Google Scholar]

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