Abstract
Humans, in particular, and to a lesser extent also other species of animals, possess the impressive capability of smoothly coordinating their actions with those of others. The great amount of work done in recent years in neuroscience has provided new insights into the processes involved in joint action, intention understanding, and task sharing. In particular, the discovery of mirror neurons, which fire both when animals execute actions and when they observe the same actions done by other individuals, has shed light on the intimate relationship between perception and action elucidating the direct contribution of motor knowledge to action understanding. Up to date, however, a detailed description of the neural processes involved in these phenomena is still mostly lacking. Building upon data from single neuron recordings in monkeys observing the actions of a demonstrator and then executing the same or a complementary action, this paper describes the functioning of a biologically constraint neural network model of the motor and mirror systems during joint action. In this model, motor sequences are encoded as independent neuronal chains that represent concatenations of elementary motor acts leading to a specific goal. Action execution and recognition are achieved through the propagation of activity within specific chains. Due to the dual property of mirror neurons, the same architecture is capable of smoothly integrating and switching between observed and self-generated action sequences, thus allowing to evaluate multiple hypotheses simultaneously, understand actions done by others, and to respond in an appropriate way.
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References
Allison T, Puce A, McCarthy G (2000) Social perception from visual cues: role of the sts region. Trends Cogn Sci 4:267–278
Bonaiuto J, Rosta E, Arbib MA (2007) Extending the mirror neuron system model, I Audible actions and invisible grasps. Biol Cybern 96:9–38
Bonini L, Rozzi S, Ugolotti F, Simone L, Ferrari PF, Fogassi L (2010) Ventral premotor and inferior parietal cortices make distinct contribution to action organization and intention understanding. Cereb Cortex 20:1372–1385
Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, Seitz RJ, Zilles K, Rizzolatti G, Freund HJ (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fmri study. Eur J Neurosci 13:400–404
Chalmeau R (1994) Do chimpanzees cooperate in a learning task? Primates 35:385–392
Chersi F, Fogassi L, Rozzi S, Rizzolatti G, Ferrari P (2005) Neuronal chains for actions in the parietal lobe: a computational model. Soc Neurosci Abs 4128
Chersi F, Mukovskiy A, Fogassi L, Ferrari PF, Erlhagen W (2006) A model of intention understanding based on learned chains of motor acts in the parietal lobe. Comput Neurosci 69:48
Chersi F, Thill S, Ziemke T, Borghi AM (2010) Sentence processing: linking language to motor chains. Front Neurorob 4:1–12
Craighero L, Metta G, Sandini G, Fadiga L (2007) The mirror-neurons system: data and models. Prog Brain Res 164:39–59
Dayan P, Abbott LF (2001) Theoretical neuroscience. Computational and mathematical modelling of neural systems. MIT Press, Cambridge
Demiris Y, Hayes G (2002) Imitation as a dual-route process featuring predictive and learning components: a biologically-plausible computational model. MIT Press, Cambridge
Di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp Brain Res 91:176–180
Fagg AH, Arbib MA (1998) Modeling parietal-premotor interactions in primate control of grasping. Neural Netw 11:1277–1303
Fogassi L, Bonini L, Simone L, Ugolotti F, Ruggeri E, Rozzi S, Chersi F, Rizzolatti G, Ferrari PF (2007) Time course of neuronal activity reflecting the final goal of observed and executed action sequences in monkey parietal and premotor cortex. Soc Neurosci Abs 636:6
Fogassi L, Ferrari P, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005a) Parietal lobe: from action organization to intention understanding. Science 308:662–667
Fogassi L, Ferrari P, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005b) Supporting material for: Parietal lobe: from action organization to intention understanding. Science 308. http://www.sciencemag.org/content/308/5722/662/suppl/DC1
Frith CD, Frith U (1999) Interacting minds—a biological basis. Science 286(5445):1692–1695
Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609
Gallese V, Fadiga L, Fogassi L, Rizzolatti G (2002) Action representation and the inferior parietal lobule. In: Prinz W, Hommel B (eds) Common mechanisms in perception and action: attention and performance. Oxford University Press, Oxford. pp 334–355
Gallese V, Keysers C, Rizzolatti G (2004) A unifying view of the basis of social cognition. Trend Cogn Sci 8:396–403
Gentilucci M, Rizzolatti G (1990) Cortical motor control of arm and hand movements. In: Goodale MA (eds) Vision and action: the control of grasping. Ablex, Norwood. pp 147–162
Grinnel J, Packer C, Pusey AE (1995) Cooperation in male lions: kinship, reciprocity, or mutualism? Animal Behav 49:95–105
Grossman E, Donnelly M, Price R, Pickens D, Morgan V, Neighbor G, Blake R (2000) Brain areas involved in perception of biological motion. J Cogn Neurosci 12:711–720
Haruno M, Wolpert DM, Kawato M (2001) Mosaic model for sensorimotor learning and control. Neural Comput 13:2201–2220
Hauber W (1998) Involvement of basal ganglia transmitter systems in movement initiation. Prog Neurobiol 45:507–540
Iacoboni M, Koski LM, Brass M, Bekkering H, Woods RP, Dubeau MC, Mazziotta JC, Rizzolatti G (2001) Reafferent copies of imitated actions in the right superior temporal cortex. Proc Natl Acad Sci USA 98(24):13995–13999
Iacoboni M, Molnar-Szakacs I, Gallese V, Buccino G, Mazziotta JC, Rizzolatti G (2005) Grasping the intentions of others with one’s own mirror neuron system. PLoS Biol 3(3):79
Luppino G, Rizzolatti G (2000) The organization of the frontal motor cortex. News Physiol Sci 15:219–224
Melis AP, Hare B, Tomasello M (2006) Chimpanzees recruit the best collaborators. Science 311:1297–1300
Nishitani N, Hari R (2000) Temporal dynamics of cortical representation for action. Proc Natl Acad Sci USA 97(2):913–918
Noe R (2006) Cooperation experiments: coordination through communication versus acting apart together. Animal Behav 71:1–18
Oram MW, Perrett DI (1994) Responses of anterior superior temporal polysensory (stpa) neurons to biological motion stimuli. J Cogn Neurosci 6:99–116
Oztop E, Arbib MA (2002) Schema design and implementation of the grasp-related mirror neuron system. Biol Cybern 87(2):116–140
Oztop E, Wolpert DM, Kawato MM (2005) Mental state inference using visual control parameters. Cogn Brain Res 22(2):129–151
Perrett D, Harries M, Bevan R, Thomas S, Benson P, Mistlin A, Chitty A, Hietanen J, Ortega J (1989) Frameworks of analysis for the neural representation of animate objects and actions. J Exp Biol 146:87–113
Rizzolatti G, Craighero L (2004) The mirror neuron system. Annual Rev Neurosci 27:169–192
Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2:661–670
Rushworth MFS, Behrens TEJ, Johansen-Berg H (2006) Connection patterns distinguish three regions of human parietal cortex. Cereb Cortex 16:1418–1430
Sebanz N, Bekkering H, Knoblich G (2006) Joint action: bodies and minds moving together. Trend Cogn Sci 10(2):70–76
Sebanz N, Knoblich G (2009) Prediction in joint action: What, when, and where. Top Cogn Sci 1:353–367
Thach WT (1975) Timing of activity in cerebellar dentate nucleus and cerebral motor cortex during prompt volitional movement. Brain Res 88:233–241
Visalberghi E, Quarantotti BP, Tranchida F (2000) Solving a cooperation task without taking into account the partner’s behavior: the case of capuchin monkeys (cebus apella). J Comp Psychol 114:297–301
Acknowledgments
A particular thank goes to Leonardo Fogassi and Pier Francesco Ferrari who gave me the opportunity to work in their laboratory at the University of Parma. This work was partially supported by the European project Artesimit, EC Grant IST-2000-29689.
Conflict of interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Chersi, F. Neural mechanisms and models underlying joint action. Exp Brain Res 211, 643–653 (2011). https://doi.org/10.1007/s00221-011-2690-3
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DOI: https://doi.org/10.1007/s00221-011-2690-3