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Article published In: How the Brain Got Language: Towards a New Road Map
Edited by Michael A. Arbib
[Interaction Studies 19:1/2] 2018
► pp. 38–53

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

 | Institut des Sciences Cognitives Marc Jeannerod – CNRS
 | Institut des Sciences Cognitives Marc Jeannerod – CNRS
Published online: 17 September 2018
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https://doi.org/10.1075/is.17037.cou
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.
Article outline
  • Introduction
  • Mirroring others’ actions and gestures through the motor system
    • Hand and mouth: Two different mirror networks
    • Processing reward and social context
    • Mouth mirror access to visual information does not occur via the parietal cortex
    • Facial gestural communication and the face mirror network
    • Hand mouth synergies
    • Hand mouth synergies for gestural communication
  • Towards a new road map
  • Acknowledgements
  • References
References (73)
References
Apps, M. A. J., Rushworth, M. F. S., Chang, S. W. C. (2016). The Anterior Cingulate Gyrus and Social Cognition: Tracking the Motivation of Others. Neuron 901, 692–707. Google Scholar logo with link to Google Scholar
Arbib, M. A. (2016). Towards a Computational Comparative Neuroprimatology: Framing the language-ready brain. Phys Life Rev 161, 1–54. Google Scholar logo with link to Google Scholar
Arbib, M. A., Liebal, K., Pika, S. (2008). Primate Vocalization, Gesture, and the Evolution of Human Language. Curr Anthropol 491, 1053–1076 Available at: [URL].
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 3691, 20130414–20130414 Available at: [URL].
Azzi, J. C. B., Sirigu, A., Duhamel, J. -R. (2012). Modulation of value representation by social context in the primate orbitofrontal cortex. Proc Natl Acad Sci 1091, 2126–2131. Google Scholar logo with link to Google Scholar
Barbas, H. (1988). Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 2761, 313–342. Google Scholar logo with link to Google Scholar
Borra, A. E., Gerbella, M., Rozzi, S., Luppino, G. (2017). The macaque lateral grasping network: a neural substrate for generating purposeful hand actions. Neurosci Biobehav Rev 751, 65–90. Google Scholar logo with link to Google Scholar
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. Brain Struct Funct 0:0. Google Scholar logo with link to Google Scholar
Cai, X., Padoa-Schioppa, C. (2012). Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex. J Neurosci 321, 3791–3808. Google Scholar logo with link to Google Scholar
Call, J., Tomasello, M. (2007). The gestural communication of apes and monkeys. (Erlbaum, L., ed). Mahwah, NJ.Google Scholar logo with link to Google Scholar
Carr, L., Iacoboni, M., Dubeau, M. -C., Mazziotta, J. C., Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci U S A 1001, 5497–5502. Google Scholar logo with link to Google Scholar
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 211, 195–199. Google Scholar logo with link to Google Scholar
Coudé, G., Ferrari, P. F., 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 61, 1–10. Google Scholar logo with link to Google Scholar
de Vignemont, F., Singer, T. (2006). The empathic brain: how, when and why? Trends Cogn Sci 101, 435–441. Google Scholar logo with link to Google Scholar
Decety, J., Jackson, P. L. (2006). A Social-Neuroscience Perspective on Empathy. Curr Dir Psychol Sci 151, 54–58 Available at: [URL].
Decety, J., Lamm, C. (2006). Human Empathy Through the Lens of Social Neuroscience. Sci World J 61, 1146–1163 Available at: [URL].
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 1111, 5718–5722 Available at: [URL].
di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., Rizzolatti, G. (1992). Understanding motor events: a neurophysiological study. Exp brain Res 911, 176–180. Google Scholar logo with link to Google Scholar
Ferrari, P. F., 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 171, 1703–1714. [Accessed June 27, 2016].Google Scholar logo with link to Google Scholar
Ferrari, P. F., Visalberghi, E., Paukner, A., Fogassi, L., Ruggiero, A., Suomi, S. (2006). Neonatal Imitation in Rhesus Macaques. PLoS Biol 41, e302. Google Scholar logo with link to Google Scholar
Ferrari, P. F. F., Gerbella, M., Coudé, G., Rozzi, S. (2017). Two different mirror neuron networks: the sensorimotor (hand) and limbic (face) pathways. Neuroscience 3581, 300–315. [URL]
Fogassi, L., Ferrari, P. (2012). Cortical Motor Organization, Mirror Neurons, and Embodied Language: An Evolutionary Perspective. Biolinguistics:308–337 Available at: [URL].
Gallese, V., Fadiga, L., Fogassi, L., Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain 1191 (Pt 21, 593–609. Google Scholar logo with link to Google Scholar
Gentilucci, M., Campione, G. C. (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. Google Scholar logo with link to Google Scholar
Gentilucci, M., Corballis, M. C. (2006). From manual gesture to speech: a gradual transition. Neurosci Biobehav Rev 301, 949–960 Available at: [URL] [Accessed August 21, 2014].
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 711, 475–490. Google Scholar logo with link to Google Scholar
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 2161, 43–65. Google Scholar logo with link to Google Scholar
Gerbella, M., Borra, E., Tonelli, S., Rozzi, S., Luppino, G. (2013). Connectional heterogeneity of the ventral part of the macaque area 46. Cereb Cortex 231, 967–987. Google Scholar logo with link to Google Scholar
Gómez, J. C. (2007). Pointing behaviors in apes and human infants: A balanced interpretation. Child Dev 781, 729–734. Google Scholar logo with link to Google Scholar
Graziano, M. S. A., Aflalo, T. N. S., Cooke, D. F. (2005). Arm movements evoked by electrical stimulation in the motor cortex of monkeys. J Neurophysiol 941, 4209–4223 Available at: [URL] [Accessed August 27, 2016].
Graziano, M. S. A., Taylor, C. S. R., Moore, T. (2002). Complex movements evoked by microstimulation of precentral cortex. Neuron 341, 841–851. Google Scholar logo with link to Google Scholar
Halina, M., Rossano, F., Tomasello, M. (2013). The ontogenetic ritualization of bonobo gestures. Anim Cogn 161, 653–666. Google Scholar logo with link to Google Scholar
Hatfield, E., Cacioppo, J., Rapson, R. (1993). Emotional Contagion. Curr Dir Psychol Sci 21, 96–99. Google Scholar logo with link to Google Scholar
Hayden, B. Y., Smith, D. V., Platt, M. L. (2010). Cognitive control signals in posterior cingulate cortex. Front Hum Neurosci 41, 223 Available at: [URL].
Hillman, K. L., Bilkey, D. K. (2012). Neural encoding of competitive effort in the anterior cingulate cortex. Nat Neurosci 151, 1290–1297 Available at: [URL][URL].
Huang, C. S., Sirisko, M. A., Hiraba, H., Murray, G. M., Sessle, B. J. (1988). Organization of the primate face motor cortex as revealed by intracortical microstimulation and electrophysiological identification of afferent inputs and corticobulbar projections. J Neurophysiol 591, 796–818 Available at: [URL] [Accessed August 27, 2016].
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 1091, 10077–10082 Available at: [URL][URL].
Kaas, J. H., Gharbawie, O. A., Stepniewska, I. (2013). Cortical networks for ethologically relevant behaviors in primates. Am J Primatol 751, 407–414. Google Scholar logo with link to Google Scholar
Keysers, C., Fadiga, L. (2008). The mirror neuron system: new frontiers. Soc Neurosci 31, 193–198. Google Scholar logo with link to Google Scholar
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 541, 2492–2502 Available at: [URL].
Leavens, D. A., Hopkins, W. D., Bard, K. A. (2005). Understanding the Point of Chimpanzee Pointing. Epigenesis and Ecological Validity. Curr Dir Psychol Sci 141, 185–189. Google Scholar logo with link to Google Scholar
Leavens, D. A., Hopkins, W. D., Thomas, R. K. (2004). Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 1181, 48–57 Available at: [URL] [Accessed July 31, 2014].
Leavens, DA, Russell, JL, Hopkins, WD. (2004b) Intentionality as Measured in the Persistence and Elaboration of Communication by Chimpanzees (Pan troglodytes). Child Dev 761:291–306. Google Scholar logo with link to Google Scholar
Liebal, K., Call, J. (2012). The origins of non-human primates’ manual gestures. Philos Trans R Soc B Biol Sci 3671, 118–128. Google Scholar logo with link to Google Scholar
Lyn, H., Greenfield, P. M., Savage-Rumbaugh, S., Gillespie-Lynch, K., Hopkins, W. D. (2011). Nonhuman primates do declare! A comparison of declarative symbol and gesture use in two children, two bonobos, and a chimpanzee. Lang Commun 311, 63–74. Google Scholar logo with link to Google Scholar
Mancini, G., Ferrari, P. F., Palagi, E. (2013) In Play We Trust. Rapid Facial Mimicry Predicts the Duration of Playful Interactions in Geladas. PLoS One 81, 2–6. Google Scholar logo with link to Google Scholar
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. Google Scholar logo with link to Google Scholar
Maranesi, M., Rodà, F., Bonini, L., Rozzi, S., Ferrari, P. F., Fogassi, L., Coudé, G. (2012). Anatomo-functional organization of the ventral primary motor and premotor cortex in the macaque monkey. Eur J Neurosci 361, 3376–3387. Google Scholar logo with link to Google Scholar
McGuinness, E., Sivertsen, D., Allman, J. M. (1980). Organization of the face representation in macaque motor cortex. J Comp Neurol 1931, 591–608 Available at: [URL] [Accessed August 27, 2016].
Morecraft, R. J., Louie, J. L., Herrick, J. L., Stilwell-Morecraft, K. S. (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 1241, 176–208. Google Scholar logo with link to Google Scholar
Nelissen, K., Vanduffel, W. (2011). Grasping-related functional magnetic resonance imaging brain responses in the macaque monkey. J Neurosci 311, 8220–8229 Available at: [URL].
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 821, 179–188. Google Scholar logo with link to Google Scholar
Oztop, E., Arbib, M. A. (2002). Schema design and implementation of the grasp-related mirror neuron system. Biol Cybern 871, 116–140. Google Scholar logo with link to Google Scholar
Preston, S. D., Waal, F. B. M. De. (2002). Preston_deWaal_2002. 1–71.Google Scholar logo with link to Google Scholar
Preston, S. D., & Waal, F. B. M. De. (2002). Empathy: Its ultimate and proximate bases. Behavioral and Brain Sciences, 25(1), 1–71. Google Scholar logo with link to Google Scholar
Rizzolatti, G., Arbib, M. A. (1998). Language within our grasp. Trends Neurosci 211, 188–195. Google Scholar logo with link to Google Scholar
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 941, 655–706. Google Scholar logo with link to Google Scholar
Rizzolatti, G., Sinigaglia, C. (2016). The mirror mechanism: a basic principle of brain function. Nat Rev Neurosci 171, 757–765 Available at: [URL] [URL].
Romanski, L. M. (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 Available at: [URL] [Accessed July 26, 2014].
Rozzi, S., Calzavara, R., Belmalih, A., Borra, E., Gregoriou, G. G., Matelli, M., Luppino, G. (2006). Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 161, 1389–1417. Google Scholar logo with link to Google Scholar
Saalmann, Y. B., Kastner, S. (2011). Cognitive and Perceptual Functions of the Visual Thalamus. Neuron 711, 209–223. Google Scholar logo with link to Google Scholar
Sherman, S. M. (2007). The thalamus is more than just a relay. Curr Opin Neurobiol 171, 417–422. Google Scholar logo with link to Google Scholar
Simone, L., Bimbi, M., Rodà, F., Fogassi, L., Rozzi, S. (2017). Action observation activates neurons of the monkey ventrolateral prefrontal cortex. Sci Rep 71, 44378 Available at: [URL].
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 421, 2882–2894. Google Scholar logo with link to Google Scholar
Singer, T. (2006). The neuronal basis and ontogeny of empathy and mind reading: Review of literature and implications for future research. Neurosci Biobehav Rev 301, 855–863. Google Scholar logo with link to Google Scholar
Singer, T., Seymour, B., O’Dohery, J., Kaube, H., Dolan, R. J., Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science (80-) 3031, 1157–1162. Google Scholar logo with link to Google Scholar
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 431, 95–104. Google Scholar logo with link to Google Scholar
Tramacere, A., Ferrari, P. F. (2016). Faces in the mirror, from the neuroscience of mimicry to the emergence of mentalizing. J Anthropol Sci 941, 113–126.Google Scholar logo with link to Google Scholar
Tramacere, A., Pievani, T., Ferrari, P. F. (2016). Mirror neurons in the tree of life: mosaic evolution, plasticity and exaptation of sensorimotor matching responses. Biol Rev:0–0.Google Scholar logo with link to Google Scholar
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 301, 1155–1170. Google Scholar logo with link to Google Scholar
van Hooff, J. R. R. A. M. (1967). The facial displays of catarrhine monkeys and apes. In: Primate Ethology, Weidenfeld. (Morris, D., ed), pp 7–68. London.Google Scholar logo with link to Google Scholar
Walter, H. (2011). Social Cognitive Neuroscience of Empathy – Concepts, circuits and genes. Neuroscience in press:9–17 Available at: [URL].
Zaki, J., Ochsner, K. N. (2012). The neuroscience of empathy: progress, pitfalls and promise. Nat Neurosci 151, 675–680. Google Scholar logo with link to Google Scholar
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