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Toward a functional account of the human mirror system
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ScienceDirect Physics of Life Reviews 12 (2015) 104–105 www.elsevier.com/locate/plrev
Comment
Toward a functional account of the human mirror system Comment on “Grasping synergies: A motor-control approach to the mirror neuron mechanism” by A. D’Ausilio et al. Peter G. Enticott Cognitive Neuroscience Unit, School of Psychology, Deakin University, 221 Burwood Highway, Burwood, Victoria, 3125, Australia Received 31 December 2014; received in revised form 11 January 2015; accepted 12 January 2015 Available online 14 January 2015 Communicated by L. Perlovsky
It has been more than 20 years since the first reports of macaque “mirror neurons” appeared in the literature [1], and a large number of studies have since established an analogous system in the human brain [2]. Despite a raft of studies using various methodological approaches, we appear to be moving further away from any form of consensus, particularly concerning what this mirror system actually “mirrors” (e.g., low-level motor representation, goal or intention coding), and the functional significance (if any) of this mechanism [3]. The conceptual issues discussed by D’Ausilio et al. [4] are indeed critical to the advancement of this field; interestingly, they suggest that examining kinematic vs. goal coding aspects of the mirror system might be redundant, and propose instead a new approach that examines the recruitment of motor synergies within the context of the mirror system. An examination of the recruitment of broad-ranging motor synergies might resolve some of the critical issues surrounding the human mirror system. Within the reviewed literature, however, there is a broader controversy: specifically, what does corticospinal excitability (CSE)-modulation during action observation reflect at a neural level? The neural origin of this signal might be seen as a separate issue, but implicit within the discussion in D’Ausilio et al.’s [4] review is the suggestion that CSE changes reflect a mirror mechanism that is underpinned by mirror neurons. This remains to be determined. It is possible that CSE changes associated with kinematic aspects and goal/object aspects arise from separate neural mechanisms. The authors have noted the temporal limitations of other techniques for indexing the mirror mechanism, but neural contributions to CSE-modulation are likely to be elucidated by integrated approaches to cognitive neuroscience, such as combined TMS-EEG and TMS-fMRI, which will place this information in a network context. Concurrent eye tracking will also be advantageous, allowing a determination of the relationship between visual attention/processing and the mirror response to further understand the visuomotor relationship within this system. Unfortunately, critical methodological problems with TMS-based approaches to the mirror system remain. Perhaps most concerning within the reviewed studies is the variability among control or “baseline” conditions (i.e., a comparator that enables the inference of a mirror response). For instance, some compare relative muscle activation within a single trial (e.g., first dorsal interosseus [FDI] vs. abductor digiti minimi [ADM] [5]), while others compare excitability between trials (e.g., CSE during action observation compared with CSE during observation of a static hand, visual DOI of original article: http://dx.doi.org/10.1016/j.plrev.2014.11.002. E-mail address: [email protected]. http://dx.doi.org/10.1016/j.plrev.2015.01.018 1571-0645/© 2015 Elsevier B.V. All rights reserved.
P.G. Enticott / Physics of Life Reviews 12 (2015) 104–105
105
white noise, or a fixation cross [6–8]). These approaches yield vastly differing indices of a mirror response. It is not clear which method would be favored in examining “mirrored” motor synergies, but this is an area in desperate need of consensus. It seems entirely valid that an approach from studies of the motor system be applied to the mirror system, and internal models could further contribute to predictive elements of mirroring [9]. The suggested approach may also be informative when considering disorders where both mirror and motor deficits have been documented, such as autism spectrum disorder [10,11]. Nevertheless, clear and testable predictions are required. For instance, should it emerge that the mirror system does indeed recruit motor synergies, it will then be important to determine whether these synergies confer a functional significance (e.g., action understanding, prediction, preparation of complementary responses), and how a mirror mechanism might interact with other networks that appear devoted to understanding others’ motor behavior [12]. Indeed, the recruitment of motor synergies during action observation can still be accommodated within an associative learning framework that might downplay any functional significance [13]. In any event, determining the precise nature of the mirror response (e.g., recruitment of motor synergies) would represent a major advance in our understanding of this system, and could have substantial explanatory power in our functional understanding of the mirror mechanism. Acknowledgements Peter G. Enticott is supported by a Career Development Fellowship (GNT1052073) from the National Health and Medical Research Council (NHMRC), Australia. References [1] di Pellegrino G, et al. Understanding motor events: a neurophysiological study. Exp Brain Res 1992;91:176–80. [2] Rizzolatti G, Sinigaglia C. The functional role of the Parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci 2010;11(4):264–74. [3] Gallese V, et al. Mirror neuron forum. Perspect Psychol Sci 2011;6(4):369–407. [4] 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]. [5] Theoret H, et al. Impaired motor facilitation during action observation in individuals with autism spectrum disorder. Curr Biol 2005;15(3):R84–5. [6] Hill AT, et al. Modulation of putative mirror neuron activity by both positively and negatively valenced affective stimuli: a TMS study. Behav Brain Res 2013:116–23. [7] Oberman LM, et al. EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cogn Brain Res 2005;24:190–8. [8] Puzzo I, et al. Reduced cortico-motor facilitation in a normal sample with high traits of autism. Neurosci Lett 2009;467(2):173–7. [9] Wolpert DM, Diedrichsen J, Flanagan JR. Principles of sensorimotor learning. Nat Rev Neurosci 2011;12(12):739–51. [10] Fournier KA, et al. Motor coordination in autism spectrum disorders: a synthesis and meta-analysis. J Autism Dev Disord 2010;40(10):1227–40. [11] Rizzolatti G, Fabbri-Destro M. Mirror neurons: from discovery to autism. Exp Brain Res 2010;200(3–4):223–37. [12] Becchio C, et al. Social grasping: from mirroring to mentalizing. NeuroImage 2012;61(1):240–8. [13] Cook R, et al. Mirror neurons: from origin to function. Behav Brain Sci 2014;37(2):177–92.
ScienceDirect Physics of Life Reviews 12 (2015) 104–105 www.elsevier.com/locate/plrev
Comment
Toward a functional account of the human mirror system Comment on “Grasping synergies: A motor-control approach to the mirror neuron mechanism” by A. D’Ausilio et al. Peter G. Enticott Cognitive Neuroscience Unit, School of Psychology, Deakin University, 221 Burwood Highway, Burwood, Victoria, 3125, Australia Received 31 December 2014; received in revised form 11 January 2015; accepted 12 January 2015 Available online 14 January 2015 Communicated by L. Perlovsky
It has been more than 20 years since the first reports of macaque “mirror neurons” appeared in the literature [1], and a large number of studies have since established an analogous system in the human brain [2]. Despite a raft of studies using various methodological approaches, we appear to be moving further away from any form of consensus, particularly concerning what this mirror system actually “mirrors” (e.g., low-level motor representation, goal or intention coding), and the functional significance (if any) of this mechanism [3]. The conceptual issues discussed by D’Ausilio et al. [4] are indeed critical to the advancement of this field; interestingly, they suggest that examining kinematic vs. goal coding aspects of the mirror system might be redundant, and propose instead a new approach that examines the recruitment of motor synergies within the context of the mirror system. An examination of the recruitment of broad-ranging motor synergies might resolve some of the critical issues surrounding the human mirror system. Within the reviewed literature, however, there is a broader controversy: specifically, what does corticospinal excitability (CSE)-modulation during action observation reflect at a neural level? The neural origin of this signal might be seen as a separate issue, but implicit within the discussion in D’Ausilio et al.’s [4] review is the suggestion that CSE changes reflect a mirror mechanism that is underpinned by mirror neurons. This remains to be determined. It is possible that CSE changes associated with kinematic aspects and goal/object aspects arise from separate neural mechanisms. The authors have noted the temporal limitations of other techniques for indexing the mirror mechanism, but neural contributions to CSE-modulation are likely to be elucidated by integrated approaches to cognitive neuroscience, such as combined TMS-EEG and TMS-fMRI, which will place this information in a network context. Concurrent eye tracking will also be advantageous, allowing a determination of the relationship between visual attention/processing and the mirror response to further understand the visuomotor relationship within this system. Unfortunately, critical methodological problems with TMS-based approaches to the mirror system remain. Perhaps most concerning within the reviewed studies is the variability among control or “baseline” conditions (i.e., a comparator that enables the inference of a mirror response). For instance, some compare relative muscle activation within a single trial (e.g., first dorsal interosseus [FDI] vs. abductor digiti minimi [ADM] [5]), while others compare excitability between trials (e.g., CSE during action observation compared with CSE during observation of a static hand, visual DOI of original article: http://dx.doi.org/10.1016/j.plrev.2014.11.002. E-mail address: [email protected]. http://dx.doi.org/10.1016/j.plrev.2015.01.018 1571-0645/© 2015 Elsevier B.V. All rights reserved.
P.G. Enticott / Physics of Life Reviews 12 (2015) 104–105
105
white noise, or a fixation cross [6–8]). These approaches yield vastly differing indices of a mirror response. It is not clear which method would be favored in examining “mirrored” motor synergies, but this is an area in desperate need of consensus. It seems entirely valid that an approach from studies of the motor system be applied to the mirror system, and internal models could further contribute to predictive elements of mirroring [9]. The suggested approach may also be informative when considering disorders where both mirror and motor deficits have been documented, such as autism spectrum disorder [10,11]. Nevertheless, clear and testable predictions are required. For instance, should it emerge that the mirror system does indeed recruit motor synergies, it will then be important to determine whether these synergies confer a functional significance (e.g., action understanding, prediction, preparation of complementary responses), and how a mirror mechanism might interact with other networks that appear devoted to understanding others’ motor behavior [12]. Indeed, the recruitment of motor synergies during action observation can still be accommodated within an associative learning framework that might downplay any functional significance [13]. In any event, determining the precise nature of the mirror response (e.g., recruitment of motor synergies) would represent a major advance in our understanding of this system, and could have substantial explanatory power in our functional understanding of the mirror mechanism. Acknowledgements Peter G. Enticott is supported by a Career Development Fellowship (GNT1052073) from the National Health and Medical Research Council (NHMRC), Australia. References [1] di Pellegrino G, et al. Understanding motor events: a neurophysiological study. Exp Brain Res 1992;91:176–80. [2] Rizzolatti G, Sinigaglia C. The functional role of the Parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci 2010;11(4):264–74. [3] Gallese V, et al. Mirror neuron forum. Perspect Psychol Sci 2011;6(4):369–407. [4] 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]. [5] Theoret H, et al. Impaired motor facilitation during action observation in individuals with autism spectrum disorder. Curr Biol 2005;15(3):R84–5. [6] Hill AT, et al. Modulation of putative mirror neuron activity by both positively and negatively valenced affective stimuli: a TMS study. Behav Brain Res 2013:116–23. [7] Oberman LM, et al. EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cogn Brain Res 2005;24:190–8. [8] Puzzo I, et al. Reduced cortico-motor facilitation in a normal sample with high traits of autism. Neurosci Lett 2009;467(2):173–7. [9] Wolpert DM, Diedrichsen J, Flanagan JR. Principles of sensorimotor learning. Nat Rev Neurosci 2011;12(12):739–51. [10] Fournier KA, et al. Motor coordination in autism spectrum disorders: a synthesis and meta-analysis. J Autism Dev Disord 2010;40(10):1227–40. [11] Rizzolatti G, Fabbri-Destro M. Mirror neurons: from discovery to autism. Exp Brain Res 2010;200(3–4):223–37. [12] Becchio C, et al. Social grasping: from mirroring to mentalizing. NeuroImage 2012;61(1):240–8. [13] Cook R, et al. Mirror neurons: from origin to function. Behav Brain Sci 2014;37(2):177–92.