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Joining forces: Motor control meets mirror neurons
Available online at www.sciencedirect.com
ScienceDirect Physics of Life Reviews 12 (2015) 111–113 www.elsevier.com/locate/plrev
Comment
Joining forces: Motor control meets mirror neurons Comment on “Grasping synergies: A motor-control approach to the mirror neuron mechanism” by D’Ausilio, Bartoli, and Maffongelli Antonino Casile a,b,∗ a Istituto Italiano di Tecnologia, Italy b Harvard Medical School, Department of Neurobiology, Warren Alpert Building, room 222, 200 Longwood Avenue, 02115 Boston, MA, USA
Received 31 December 2014; accepted 31 December 2014 Available online 14 January 2015 Communicated by L. Perlovsky
Several consistent and compelling experimental findings suggest that in primates the observation of actions or movements activates the observer’s motor cortex (for a recent and very thorough review see [1]). One important piece of evidence was the discovery of mirror neurons, that are neurons in the macaque ventral pre-motor (area F5), motor and parietal cortices (area PFG) that respond both when the monkey executes a goal-directed motor act (e.g. breaking a peanut) or when it sees a similar action executed by others [2–5]. A similar system has been later reported also in humans ([6–8] but see also [9,10] for negative results). The activation of motor cortex during action observation is puzzling for two reasons. First, motor cortex is functionally defined as the part of cortex that is active during the execution or planning of movements. Thus, the fact that it possesses also visual responses requires, at least, a change in its functional definition. Second, neurons have been reported in the temporal cortex that are selectively activated during the observation of bodily movements and have no motor response [11]. Thus, in principle, the primate brain could carry out an analysis of others’ actions based only on visual cues with no involvement of motor processes. The question is thus: Why in the primate brain motor processes are active during the visual perception of the actions of others? An influential proposal by Rizzolatti and colleagues holds that mirror neurons mediate action understanding and imitation by matching the visual representations of observed actions onto their motor representations [2,12]. This proposal postulates a functional and a cognitive role for mirror neurons. The functional role is that they act as a “translation mechanism” between motor and visual representations of actions. The cognitive role is that they subserve action understanding. The proposal that the mirror-neuron system might have a role in action understanding produced quite some excitement in the scientific community (and in particular in the field of cognitive neuroscience) as it had the potential to provide a simple mechanism for a quite complex task (i.e. understanding the actions of others). However, despite almost two decades of intense research, it is not incorrect to say that we have no conclusive evidence that the mirror-neuron system has any causal role in action understanding. DOI of original article: http://dx.doi.org/10.1016/j.plrev.2014.11.002. * Correspondence to: Harvard Medical School, Department of Neurobiology, Warren Alpert Building, room 222, 200 Longwood Avenue, 02115
Boston, MA, USA. E-mail address: [email protected]. http://dx.doi.org/10.1016/j.plrev.2015.01.003 1571-0645/© 2015 Elsevier B.V. All rights reserved.
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A. Casile / Physics of Life Reviews 12 (2015) 111–113
The liveliness of the debate concerning the potential functional role of the monkey and (putative) human mirrorneuron system is vividly portrayed in several recent papers [13,14]. With respect to this debate the contribution by D’Ausilio et al. [15] is very timely and interesting for two reasons. First, it draws a very nice parallel between motor control and the mirror-neurons field. Indeed, the field of motor control has been dealing for decades with the problem of giving a functional interpretation to the discharges of neurons in motor cortex during the execution of actions. As correctly noted by D’Ausilio et al., the mirror-neurons field deals with a complementary problem. That is, to give a functional interpretation to the responses of the same areas during the observation of actions. Given this complementarity of goals, it would have seemed natural for scientists investigating the mirror-neuron system (in both humans and monkeys) to draw from previous results in the field of motor control. Strangely, that was not the case and the two communities have been working so far with basically no interaction or even mutual knowledge. With this respect, D’Ausilio et al.’s paper represents a timely invitation to scientists in the mirror-neurons field to “bridge the gap” with the field of motor control. Of course, theoretical and experimental methodologies developed in motor control might not be readily applicable to the investigation of mirror-neuron responses. Nonetheless, as proposed by D’Ausilio et al., they might provide the “fresh blood” of novel research questions and directions to our field. Second, D’Ausilio et al.’s paper provides an alternative, and very elegant, route to tackle the question of the functional role of the mirror-neuron system. More specifically, the authors propose a bottom-up approach that relates the responses of mirror neurons to the decoding of motor synergies during action observation. This proposal is vaguely reminiscent of that by Rizzolatti and co-workers stating that mirror neurons represent a translation mechanism between motor and visual representations. Adding to that, D’Ausilio et al. provide a novel hypothesis about the nature of the representations being encoded and a more solid theoretical foundation to their proposal. A potential caveat to the proposal by D’Ausilio et al. is that, similar to the mirror-neuron field, also the field of motor control faces the problem that despite several decades of research there is still no general consensus about the very role of the motor cortex [16–21]. The encoding of motor synergies is only one, albeit influential, proposal and alternative proposals exist (see, for example, [22]). Thus, there is the possibility that motor synergies might turn out not to be the correct “granularity” (to use D’Ausilio et al.’s terminology) at which to read the neuronal code of mirror neurons. Nonetheless, the direction proposed by D’Ausilio et al. looks promising and it fully deserves to be comprehensively explored as it has truly the potential to provide a novel view of the functional role of the mirror-neuron system. References [1] Rizzolatti G, Cattaneo L, Fabbri-Destro M, Rozzi S. Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiol Rev 2014;94:655–706. http://dx.doi.org/10.1152/physrev.00009.2013. [2] Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recognition in the premotor cortex. Brain 1996;119:593–609. [3] Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G. Parietal lobe: from action organization to intention understanding. Science 2005;80(308):662–7. [4] Casile A. Mirror neurons (and beyond) in the macaque brain: an overview of 20 years of research. Neurosci Lett 2013;540:3–14. http://dx.doi.org/10.1016/j.neulet.2012.11.003. [5] Dushanova J, Donoghue J. Neurons in primary motor cortex engaged during action observation. Eur J Neurosci 2010;31:386–98. http://dx.doi.org/10.1111/j.1460-9568.2009.07067.x. [6] Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 1995;73:2608–11. [7] Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G. Cortical mechanisms of human imitation. Science 1999;80(286):2526. [8] Rizzolatti G, Fadiga L, Matelli M, Bettinardi V. Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp Brain Res 1996;111:246–52. [9] Dinstein I, Gardner JL, Jazayeri M, Heeger DJ. Executed and observed movements have different distributed representations in human aIPS. J Neurosci 2008;28:11231–9. http://dx.doi.org/10.1523/JNEUROSCI.3585-08.2008. [10] Lingnau A, Gesierich B, Caramazza A. Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans. Proc Natl Acad Sci USA 2009;106:9925–30. http://dx.doi.org/10.1073/pnas.0902262106. [11] Jellema T, Perrett DI. Neural basis for the perception of goal-directed actions. In: Easton A, Emery N, editors. Cognitive neuroscience of social behaviour. Psychology Press; 2005. p. 81–112. [12] Rizzolatti G, Fogassi L, Gallese V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2001;2:661–70. http://dx.doi.org/10.1038/35090060. [13] Cook R, Bird G, Catmur C, Press C, Heyes C. Mirror neurons: from origin to function. Behav Brain Sci 2014;37:177–92. http://dx.doi.org/10.1017/S0140525X13000903.
A. Casile / Physics of Life Reviews 12 (2015) 111–113
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[14] Sinigaglia C, Hickok G. Clarifying the role of the mirror system. Neurosci Lett 2013;540:62–6. [15] D’Ausilio A, Bartoli E, Maffongelli L. Grasping synergies: a motor-control approach to the mirror neuron mechanism. Phys Life Rev 2015;12:91–103 [in this issue]. [16] Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 1982;2:1527–37. [17] Mussa-Ivaldi FA. Do neurons in the motor cortex encode movement direction? An alternative hypothesis. Neurosci Lett 1988;91:106–11. [18] Todorov E. Direct cortical control of muscle activation in voluntary arm movements: a model. Nat Neurosci 2000;3:391–8. http://dx.doi.org/10.1038/73964. [19] Scott SH. Inconvenient truths about neural processing in primary motor cortex. J Physiol 2008;586:1217–24. http://dx.doi.org/10.1113/jphysiol.2007.146068. [20] Churchland MM, Shenoy KV. Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. J Neurophysiol 2007;97:4235–57. http://dx.doi.org/10.1152/jn.00095.2007. [21] Graziano M. The organization of behavioral repertoire in motor cortex. Annu Rev Neurosci 2006;29:105–34. http://dx.doi.org/10.1146/annurev.neuro.29.051605.112924. [22] Shenoy KV, Sahani M, Churchland MM. Cortical control of arm movements: a dynamical systems perspective. Annu Rev Neurosci 2013;36:337–59. http://dx.doi.org/10.1146/annurev-neuro-062111-150509.
ScienceDirect Physics of Life Reviews 12 (2015) 111–113 www.elsevier.com/locate/plrev
Comment
Joining forces: Motor control meets mirror neurons Comment on “Grasping synergies: A motor-control approach to the mirror neuron mechanism” by D’Ausilio, Bartoli, and Maffongelli Antonino Casile a,b,∗ a Istituto Italiano di Tecnologia, Italy b Harvard Medical School, Department of Neurobiology, Warren Alpert Building, room 222, 200 Longwood Avenue, 02115 Boston, MA, USA
Received 31 December 2014; accepted 31 December 2014 Available online 14 January 2015 Communicated by L. Perlovsky
Several consistent and compelling experimental findings suggest that in primates the observation of actions or movements activates the observer’s motor cortex (for a recent and very thorough review see [1]). One important piece of evidence was the discovery of mirror neurons, that are neurons in the macaque ventral pre-motor (area F5), motor and parietal cortices (area PFG) that respond both when the monkey executes a goal-directed motor act (e.g. breaking a peanut) or when it sees a similar action executed by others [2–5]. A similar system has been later reported also in humans ([6–8] but see also [9,10] for negative results). The activation of motor cortex during action observation is puzzling for two reasons. First, motor cortex is functionally defined as the part of cortex that is active during the execution or planning of movements. Thus, the fact that it possesses also visual responses requires, at least, a change in its functional definition. Second, neurons have been reported in the temporal cortex that are selectively activated during the observation of bodily movements and have no motor response [11]. Thus, in principle, the primate brain could carry out an analysis of others’ actions based only on visual cues with no involvement of motor processes. The question is thus: Why in the primate brain motor processes are active during the visual perception of the actions of others? An influential proposal by Rizzolatti and colleagues holds that mirror neurons mediate action understanding and imitation by matching the visual representations of observed actions onto their motor representations [2,12]. This proposal postulates a functional and a cognitive role for mirror neurons. The functional role is that they act as a “translation mechanism” between motor and visual representations of actions. The cognitive role is that they subserve action understanding. The proposal that the mirror-neuron system might have a role in action understanding produced quite some excitement in the scientific community (and in particular in the field of cognitive neuroscience) as it had the potential to provide a simple mechanism for a quite complex task (i.e. understanding the actions of others). However, despite almost two decades of intense research, it is not incorrect to say that we have no conclusive evidence that the mirror-neuron system has any causal role in action understanding. DOI of original article: http://dx.doi.org/10.1016/j.plrev.2014.11.002. * Correspondence to: Harvard Medical School, Department of Neurobiology, Warren Alpert Building, room 222, 200 Longwood Avenue, 02115
Boston, MA, USA. E-mail address: [email protected]. http://dx.doi.org/10.1016/j.plrev.2015.01.003 1571-0645/© 2015 Elsevier B.V. All rights reserved.
112
A. Casile / Physics of Life Reviews 12 (2015) 111–113
The liveliness of the debate concerning the potential functional role of the monkey and (putative) human mirrorneuron system is vividly portrayed in several recent papers [13,14]. With respect to this debate the contribution by D’Ausilio et al. [15] is very timely and interesting for two reasons. First, it draws a very nice parallel between motor control and the mirror-neurons field. Indeed, the field of motor control has been dealing for decades with the problem of giving a functional interpretation to the discharges of neurons in motor cortex during the execution of actions. As correctly noted by D’Ausilio et al., the mirror-neurons field deals with a complementary problem. That is, to give a functional interpretation to the responses of the same areas during the observation of actions. Given this complementarity of goals, it would have seemed natural for scientists investigating the mirror-neuron system (in both humans and monkeys) to draw from previous results in the field of motor control. Strangely, that was not the case and the two communities have been working so far with basically no interaction or even mutual knowledge. With this respect, D’Ausilio et al.’s paper represents a timely invitation to scientists in the mirror-neurons field to “bridge the gap” with the field of motor control. Of course, theoretical and experimental methodologies developed in motor control might not be readily applicable to the investigation of mirror-neuron responses. Nonetheless, as proposed by D’Ausilio et al., they might provide the “fresh blood” of novel research questions and directions to our field. Second, D’Ausilio et al.’s paper provides an alternative, and very elegant, route to tackle the question of the functional role of the mirror-neuron system. More specifically, the authors propose a bottom-up approach that relates the responses of mirror neurons to the decoding of motor synergies during action observation. This proposal is vaguely reminiscent of that by Rizzolatti and co-workers stating that mirror neurons represent a translation mechanism between motor and visual representations. Adding to that, D’Ausilio et al. provide a novel hypothesis about the nature of the representations being encoded and a more solid theoretical foundation to their proposal. A potential caveat to the proposal by D’Ausilio et al. is that, similar to the mirror-neuron field, also the field of motor control faces the problem that despite several decades of research there is still no general consensus about the very role of the motor cortex [16–21]. The encoding of motor synergies is only one, albeit influential, proposal and alternative proposals exist (see, for example, [22]). Thus, there is the possibility that motor synergies might turn out not to be the correct “granularity” (to use D’Ausilio et al.’s terminology) at which to read the neuronal code of mirror neurons. Nonetheless, the direction proposed by D’Ausilio et al. looks promising and it fully deserves to be comprehensively explored as it has truly the potential to provide a novel view of the functional role of the mirror-neuron system. References [1] Rizzolatti G, Cattaneo L, Fabbri-Destro M, Rozzi S. Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiol Rev 2014;94:655–706. http://dx.doi.org/10.1152/physrev.00009.2013. [2] Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recognition in the premotor cortex. Brain 1996;119:593–609. [3] Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G. Parietal lobe: from action organization to intention understanding. Science 2005;80(308):662–7. [4] Casile A. Mirror neurons (and beyond) in the macaque brain: an overview of 20 years of research. Neurosci Lett 2013;540:3–14. http://dx.doi.org/10.1016/j.neulet.2012.11.003. [5] Dushanova J, Donoghue J. Neurons in primary motor cortex engaged during action observation. Eur J Neurosci 2010;31:386–98. http://dx.doi.org/10.1111/j.1460-9568.2009.07067.x. [6] Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 1995;73:2608–11. [7] Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G. Cortical mechanisms of human imitation. Science 1999;80(286):2526. [8] Rizzolatti G, Fadiga L, Matelli M, Bettinardi V. Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp Brain Res 1996;111:246–52. [9] Dinstein I, Gardner JL, Jazayeri M, Heeger DJ. Executed and observed movements have different distributed representations in human aIPS. J Neurosci 2008;28:11231–9. http://dx.doi.org/10.1523/JNEUROSCI.3585-08.2008. [10] Lingnau A, Gesierich B, Caramazza A. Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans. Proc Natl Acad Sci USA 2009;106:9925–30. http://dx.doi.org/10.1073/pnas.0902262106. [11] Jellema T, Perrett DI. Neural basis for the perception of goal-directed actions. In: Easton A, Emery N, editors. Cognitive neuroscience of social behaviour. Psychology Press; 2005. p. 81–112. [12] Rizzolatti G, Fogassi L, Gallese V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2001;2:661–70. http://dx.doi.org/10.1038/35090060. [13] Cook R, Bird G, Catmur C, Press C, Heyes C. Mirror neurons: from origin to function. Behav Brain Sci 2014;37:177–92. http://dx.doi.org/10.1017/S0140525X13000903.
A. Casile / Physics of Life Reviews 12 (2015) 111–113
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[14] Sinigaglia C, Hickok G. Clarifying the role of the mirror system. Neurosci Lett 2013;540:62–6. [15] D’Ausilio A, Bartoli E, Maffongelli L. Grasping synergies: a motor-control approach to the mirror neuron mechanism. Phys Life Rev 2015;12:91–103 [in this issue]. [16] Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 1982;2:1527–37. [17] Mussa-Ivaldi FA. Do neurons in the motor cortex encode movement direction? An alternative hypothesis. Neurosci Lett 1988;91:106–11. [18] Todorov E. Direct cortical control of muscle activation in voluntary arm movements: a model. Nat Neurosci 2000;3:391–8. http://dx.doi.org/10.1038/73964. [19] Scott SH. Inconvenient truths about neural processing in primary motor cortex. J Physiol 2008;586:1217–24. http://dx.doi.org/10.1113/jphysiol.2007.146068. [20] Churchland MM, Shenoy KV. Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. J Neurophysiol 2007;97:4235–57. http://dx.doi.org/10.1152/jn.00095.2007. [21] Graziano M. The organization of behavioral repertoire in motor cortex. Annu Rev Neurosci 2006;29:105–34. http://dx.doi.org/10.1146/annurev.neuro.29.051605.112924. [22] Shenoy KV, Sahani M, Churchland MM. Cortical control of arm movements: a dynamical systems perspective. Annu Rev Neurosci 2013;36:337–59. http://dx.doi.org/10.1146/annurev-neuro-062111-150509.