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The mirror or portrait neuron system – Time for a more organic model of action-coding?
c o r t e x 4 9 ( 2 0 1 3 ) 2 9 6 2 e2 9 6 3
Available online at www.sciencedirect.com
Journal homepage: www.elsevier.com/locate/cortex
Discussion forum
The mirror or portrait neuron system e Time for a more organic model of action-coding? Justin H.G. Williams University of Aberdeen, Mental Health, Clinical Research Centre, Cornhill Rd., Aberdeen, Aberdeenshire AB25 2ZH, United Kingdom
Since Rizzolatti et al. (1996) referred to these neurons as having ‘mirror’ properties, they have been controversial. Whilst their discovery constitutes a major contribution to social neuroscience, calling them ‘mirror neurons’ has ultimately proved unhelpful. A mirror is a piece of silvered glass that creates an exact copy of a directly perceived image. The term ‘mirror neuron’ implies that the brain projects an image of a perceived action onto the motor system, which somehow creates, through an immediate and automatic process, a motoric coding for that same action. If only this was the case! I could become an Olympic ice-skater or a concert pianist! This may be taken as a wilful misunderstanding since the claim is only that mirrors occur for basic components which can then be resequenced and developed to make sensorimotor connections for more complex actions (Buccino et al., 2004; Heyes, 2001). But it is important to emphasise just how many steps there are between copying a single small action and adopting each others’ patterns of social behaviour. If we consider this as an iterative developmental process, then images of actions, that are formed within action-coding groups of neurons, are created over time, and are slowly and iteratively developed more like painted portraits, albeit animated ones. Images are developed brush-stroke by brushstroke over a long period of observation, and each image is subject to the perspective, style and past experience of the painter. It is the very fact that each person’s animated ‘portraits’ of their action experiences are unique that makes humans such an interesting species, and which provides our culture with so much diversity. But what does a ‘portraiture’ view of actioncoding imply about social cognition? Shortly after mirror neurons were reported to exist, arguments were made that they could form the basis for a ‘simulation theory of mind’ (Gallese and Goldman, 1998) by which the idea was further
promoted that photocopying mechanisms in the brain could exist for all manner of complex actions in order for us to understand each other. A portraiture view of action-coding suggests that simulation might be a much more messy affair and action perception is subject to all sorts of biases, errors and subjective judgements. These determine our individualised perceptions of one another with consequences for our (often mistaken) mental state attributions to one another. Furthermore, if we vary between each other in the way that our motor systems function, this is likely to have a significant impact on the way that we develop our portraits of others’ actions. An example might be the way that the motor system is modulated by the limbic system in autism. The mirror neuron system is an adaptation of goal-directed learning (Rizzolatti and Arbib, 1998). The neural mechanisms for reach-to-grasp are well described in humans and primates, whereby visual feedback during action-execution is used to modify the motor planning programs (Wolpert et al., 2003). Across many species, systems for goal-directed action are closely connected to the amygdala-orbitofrontal circuit which is central to emotional learning (Kringelbach and Rolls, 2004). Social learning can come about if actions executed by others are perceived and through the mirror neuron system, elicit motor memories of similar actions. If the model and observer share similar goals, then the observed action can enhance the motor repertoire and influence motor planning and learning. It follows that such a social learning system will be very much affected by the concomitant functioning of the amygdala-orbitofrontal circuit. And hence, the nature of the relationship between limbic system and motor system is likely to be important for the way that we ‘paint’ other people’s actions. Williams et al. (2001) originally proposed that a problem with the mirror neuron system could lie at the beginning of a
E-mail address: [email protected]. 0010-9452/$ e see front matter ª 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.cortex.2013.05.005
c o r t e x 4 9 ( 2 0 1 3 ) 2 9 6 2 e2 9 6 3
2963
copy actions (echolalia and echopraxia) that are enacted with high levels of fidelity but irrespective of their own set of goals. We see competence for learning single actions, especially when they are repeated over and over. However, we also see action-learning that struggles to form organised, self-focussed and coherent action-patterns at a higher level, which are necessary for social learning, motor planning and flexible behaviour. Perhaps it is time to move forward in our thinking about the mirror (or portrait) neuron system, to a more organic and less mechanical model, that can begin to help us understand the diverse ways by which we perceive action, construct our personalised representations of action, and the problems that emerge when this learning is restricted or biased.
references Fig. 1 e Interaction between group contrast [ASD vs control] and [action imitation vs other action execution] as described by Williams et al. (2006) (Table 6). Peak at L8, 35, L2; p < .001 uncorrected, in ventromedial orbitofrontal cortex.
developmental cascade that resulted in an impairment of social learning. This was because of a pattern of abnormalities well described in autism that included poor development of theory of mind, executive function (including joint attention) and imitation. The presence of stereotyped patterns of social learning in autism, in the form of echolalia, stereotyped speech and echopraxia led them to propose a dysregulation of the mirror neuron system (rather than a ‘broken mirror’ as was suggested later by others). An empirical study of imitation in autism (Williams et al., 2006) found reduced mirror neuron system activity in autism, but also reduced modulation of the amygdala-orbitofrontal circuit during imitation. This included reduced activity in ventromedial prefrontal cortex during imitation compared to a control goal-directed visuomotor learning condition (Fig. 1). This aspect of ventromedial prefrontal cortex is thought to serve flexible reward-dependent learning (Kringelbach and Rolls, 2004), which might be taken as reason to suggest that ultimately, the problems of social learning in autism are motivational (Chevallier et al., 2012). However, social learning may just be less flexible. During typical development social learning takes place in a context by which observed behaviour is evaluated and its worth considered before it is incorporated into the behaviour repertoire. A child evaluates others’ behaviour and determines whether it is going to help him or her reach desired goals. If it is, it can then be incorporated appropriately into the specific repertoire for that goal. In autism (as well as some neurological and other neurodevelopmental conditions), we see children attempt to
Buccino G, Vogt S, Ritzl A, Fink GR, Zilles K, Freund HJ, et al. Neural circuits underlying imitation learning of hand actions: An event-related fMRI study. Neuron, 42(2): 323e334, 2004. Chevallier C, Kohls G, Troiani V, Brodkin ES, and Schultz RT. The social motivation theory of autism. Trends in Cognitive Sciences, 16(4): 231e239, 2012. Gallese V and Goldman A. Mirror neurons and the simulation theory of mind-reading. Trends in Cognitive Sciences, 2: 493e501, 1998. Heyes C. Causes and consequences of imitation. Trends in Cognitive Sciences, 5(6): 253e261, 2001. Kringelbach ML and Rolls ET. The functional neuroanatomy of the human orbitofrontal cortex: Evidence from neuroimaging and neuropsychology. Progress in Neurobiology, 72(5): 341e372, 2004. Rizzolatti G and Arbib MA. Language within our grasp. Trends in Neurosciences, 21(5): 188e194, 1998. Rizzolatti G, Fadiga L, Gallese V, and Fogassi L. Premotor cortex and the recognition of motor actions. Brain Research Cognitive Brain Research, 3(2): 131e141, 1996. Williams JH, Whiten A, Suddendorf T, and Perrett DI. Imitation, mirror neurons and autism. Neurosciences Biobehavioral Reviews, 25(4): 287e295, 2001. Williams JHG, Waiter GD, Gilchrist A, Perrett DI, Murray AD, and Whiten A. Neural mechanisms of imitation and ’mirror neuron’ functioning in autistic spectrum disorder. Neuropsychologia, 44(4): 608e619, 2006. Wolpert DM, Doya K, and Kawato M. A unifying computational framework for motor control and social interaction. Philosophical Transactions of the Royal Society of London Series BBiological Sciences, 358(1431): 593e602, 2003.
Received 23 January Reviewed 15 March Revised 4 April Accepted 9 May Published online 11 June
2013 2013 2013 2013 2013
Available online at www.sciencedirect.com
Journal homepage: www.elsevier.com/locate/cortex
Discussion forum
The mirror or portrait neuron system e Time for a more organic model of action-coding? Justin H.G. Williams University of Aberdeen, Mental Health, Clinical Research Centre, Cornhill Rd., Aberdeen, Aberdeenshire AB25 2ZH, United Kingdom
Since Rizzolatti et al. (1996) referred to these neurons as having ‘mirror’ properties, they have been controversial. Whilst their discovery constitutes a major contribution to social neuroscience, calling them ‘mirror neurons’ has ultimately proved unhelpful. A mirror is a piece of silvered glass that creates an exact copy of a directly perceived image. The term ‘mirror neuron’ implies that the brain projects an image of a perceived action onto the motor system, which somehow creates, through an immediate and automatic process, a motoric coding for that same action. If only this was the case! I could become an Olympic ice-skater or a concert pianist! This may be taken as a wilful misunderstanding since the claim is only that mirrors occur for basic components which can then be resequenced and developed to make sensorimotor connections for more complex actions (Buccino et al., 2004; Heyes, 2001). But it is important to emphasise just how many steps there are between copying a single small action and adopting each others’ patterns of social behaviour. If we consider this as an iterative developmental process, then images of actions, that are formed within action-coding groups of neurons, are created over time, and are slowly and iteratively developed more like painted portraits, albeit animated ones. Images are developed brush-stroke by brushstroke over a long period of observation, and each image is subject to the perspective, style and past experience of the painter. It is the very fact that each person’s animated ‘portraits’ of their action experiences are unique that makes humans such an interesting species, and which provides our culture with so much diversity. But what does a ‘portraiture’ view of actioncoding imply about social cognition? Shortly after mirror neurons were reported to exist, arguments were made that they could form the basis for a ‘simulation theory of mind’ (Gallese and Goldman, 1998) by which the idea was further
promoted that photocopying mechanisms in the brain could exist for all manner of complex actions in order for us to understand each other. A portraiture view of action-coding suggests that simulation might be a much more messy affair and action perception is subject to all sorts of biases, errors and subjective judgements. These determine our individualised perceptions of one another with consequences for our (often mistaken) mental state attributions to one another. Furthermore, if we vary between each other in the way that our motor systems function, this is likely to have a significant impact on the way that we develop our portraits of others’ actions. An example might be the way that the motor system is modulated by the limbic system in autism. The mirror neuron system is an adaptation of goal-directed learning (Rizzolatti and Arbib, 1998). The neural mechanisms for reach-to-grasp are well described in humans and primates, whereby visual feedback during action-execution is used to modify the motor planning programs (Wolpert et al., 2003). Across many species, systems for goal-directed action are closely connected to the amygdala-orbitofrontal circuit which is central to emotional learning (Kringelbach and Rolls, 2004). Social learning can come about if actions executed by others are perceived and through the mirror neuron system, elicit motor memories of similar actions. If the model and observer share similar goals, then the observed action can enhance the motor repertoire and influence motor planning and learning. It follows that such a social learning system will be very much affected by the concomitant functioning of the amygdala-orbitofrontal circuit. And hence, the nature of the relationship between limbic system and motor system is likely to be important for the way that we ‘paint’ other people’s actions. Williams et al. (2001) originally proposed that a problem with the mirror neuron system could lie at the beginning of a
E-mail address: [email protected]. 0010-9452/$ e see front matter ª 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.cortex.2013.05.005
c o r t e x 4 9 ( 2 0 1 3 ) 2 9 6 2 e2 9 6 3
2963
copy actions (echolalia and echopraxia) that are enacted with high levels of fidelity but irrespective of their own set of goals. We see competence for learning single actions, especially when they are repeated over and over. However, we also see action-learning that struggles to form organised, self-focussed and coherent action-patterns at a higher level, which are necessary for social learning, motor planning and flexible behaviour. Perhaps it is time to move forward in our thinking about the mirror (or portrait) neuron system, to a more organic and less mechanical model, that can begin to help us understand the diverse ways by which we perceive action, construct our personalised representations of action, and the problems that emerge when this learning is restricted or biased.
references Fig. 1 e Interaction between group contrast [ASD vs control] and [action imitation vs other action execution] as described by Williams et al. (2006) (Table 6). Peak at L8, 35, L2; p < .001 uncorrected, in ventromedial orbitofrontal cortex.
developmental cascade that resulted in an impairment of social learning. This was because of a pattern of abnormalities well described in autism that included poor development of theory of mind, executive function (including joint attention) and imitation. The presence of stereotyped patterns of social learning in autism, in the form of echolalia, stereotyped speech and echopraxia led them to propose a dysregulation of the mirror neuron system (rather than a ‘broken mirror’ as was suggested later by others). An empirical study of imitation in autism (Williams et al., 2006) found reduced mirror neuron system activity in autism, but also reduced modulation of the amygdala-orbitofrontal circuit during imitation. This included reduced activity in ventromedial prefrontal cortex during imitation compared to a control goal-directed visuomotor learning condition (Fig. 1). This aspect of ventromedial prefrontal cortex is thought to serve flexible reward-dependent learning (Kringelbach and Rolls, 2004), which might be taken as reason to suggest that ultimately, the problems of social learning in autism are motivational (Chevallier et al., 2012). However, social learning may just be less flexible. During typical development social learning takes place in a context by which observed behaviour is evaluated and its worth considered before it is incorporated into the behaviour repertoire. A child evaluates others’ behaviour and determines whether it is going to help him or her reach desired goals. If it is, it can then be incorporated appropriately into the specific repertoire for that goal. In autism (as well as some neurological and other neurodevelopmental conditions), we see children attempt to
Buccino G, Vogt S, Ritzl A, Fink GR, Zilles K, Freund HJ, et al. Neural circuits underlying imitation learning of hand actions: An event-related fMRI study. Neuron, 42(2): 323e334, 2004. Chevallier C, Kohls G, Troiani V, Brodkin ES, and Schultz RT. The social motivation theory of autism. Trends in Cognitive Sciences, 16(4): 231e239, 2012. Gallese V and Goldman A. Mirror neurons and the simulation theory of mind-reading. Trends in Cognitive Sciences, 2: 493e501, 1998. Heyes C. Causes and consequences of imitation. Trends in Cognitive Sciences, 5(6): 253e261, 2001. Kringelbach ML and Rolls ET. The functional neuroanatomy of the human orbitofrontal cortex: Evidence from neuroimaging and neuropsychology. Progress in Neurobiology, 72(5): 341e372, 2004. Rizzolatti G and Arbib MA. Language within our grasp. Trends in Neurosciences, 21(5): 188e194, 1998. Rizzolatti G, Fadiga L, Gallese V, and Fogassi L. Premotor cortex and the recognition of motor actions. Brain Research Cognitive Brain Research, 3(2): 131e141, 1996. Williams JH, Whiten A, Suddendorf T, and Perrett DI. Imitation, mirror neurons and autism. Neurosciences Biobehavioral Reviews, 25(4): 287e295, 2001. Williams JHG, Waiter GD, Gilchrist A, Perrett DI, Murray AD, and Whiten A. Neural mechanisms of imitation and ’mirror neuron’ functioning in autistic spectrum disorder. Neuropsychologia, 44(4): 608e619, 2006. Wolpert DM, Doya K, and Kawato M. A unifying computational framework for motor control and social interaction. Philosophical Transactions of the Royal Society of London Series BBiological Sciences, 358(1431): 593e602, 2003.
Received 23 January Reviewed 15 March Revised 4 April Accepted 9 May Published online 11 June
2013 2013 2013 2013 2013