Does apraxia support spatial and kinematic or mirror neuron approaches to social interaction? A commentary on Binder et al. (2017)

Accepted Manuscript Does apraxia support spatial and kinematic or mirror neuron approaches to social interaction? A commentary on Binder et al. (2017) Arran T. Reader, Matteo Candidi PII:

S0010-9452(17)30366-0

DOI:

10.1016/j.cortex.2017.10.018

Reference:

CORTEX 2167

To appear in:

Cortex

Received Date: 2 June 2017 Revised Date:

22 August 2017

Accepted Date: 21 October 2017

Please cite this article as: Reader AT, Candidi M, Does apraxia support spatial and kinematic or mirror neuron approaches to social interaction? A commentary on Binder et al. (2017), CORTEX (2017), doi: 10.1016/j.cortex.2017.10.018. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Does apraxia support spatial and kinematic or mirror neuron approaches to social interaction? A commentary on Binder et al. (2017) Arran T. Reader1* & Matteo Candidi2,3

Language Sciences, University of Reading, Reading, UK

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1. Centre for Integrative Neuroscience and Neurodynamics, School of Psychology and Clinical

2. Department of Psychology, Sapienza University of Rome, Rome, Italy 3. IRCCS, Fondazione Santa Lucia, Rome, Italy

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*Corresponding author: Arran T. Reader, School of Psychology and Clinical Language Sciences, University of Reading, Earley Gate, Whiteknights Road, Reading, RG6 6AL, UK.

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Telephone: +44 (0)118 378 8522. E-mail: [email protected]

Acknowledgements: This submission was supported by the Economic and Social Research

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Council (grant number ES/J500148/1 to ATR).

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In a recent article in Cortex Binder et al. (2017) present data from 44 left-hemisphere stroke

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patients with (n = 18) and without (n = 26) apraxia. They tested these patients, alongside healthy

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controls (n = 19), on three experimental tasks (meaningful gesture recognition, comprehension, and

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imitation), and two control tasks (control recognition, control comprehension). They also performed

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a voxel-based lesion-symptom mapping (VLSM) in order to associate lesion locations with

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experimental task performance in patients. They were specifically interested in examining whether

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regions associated with the putative human mirror neuron system (MNS) are involved critically, and

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to a similar degree, in recognising, understanding, and imitating actions.

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Their results showed that apraxic patients were significantly worse than non-apraxic patients

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and healthy controls in gesture comprehension, gesture imitation, gesture recognition, as well as in

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the control recognition task (in which participants had to decide in which of two gestures the hand

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was closer to the head). Performance in the three experimental tasks was significantly correlated.

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Defective gesture comprehension was associated with cortical lesions in the operculum, insula, and

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inferior frontal gyrus (IFG), whilst defective gesture imitation was associated with cortical lesions

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in the postcentral gyrus, middle temporal gyrus, superior temporal gyrus, intraparietal sulcus,

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supramarginal gyrus, operculum, and insula. The authors state that the deficits in gesture

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comprehension are mainly associated with anterior regions of the MNS (IFG), whilst gesture

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imitation deficits are associated with the posterior MNS (inferior parietal lobule, superior temporal

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sulcus). They conclude that their data “not only support the notion of [a MNS], but characterize its

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functional role by showing its relevance for action comprehension and imitation” (p. 135).

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The putative human frontoparietal MNS has strongly influenced discussions of social

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interaction (Cook & Bird, 2013; Hamilton, 2014; Kilner & Lemon, 2013; Press & Cook, 2015), and

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Binder et al. (2017) are right to bridge the gap between studies of social interaction in healthy

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people and neuropsychological research. Whilst we recognise that simulative comparisons between

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observed and stored actions may have a role to play in action comprehension and imitation, and that

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these processes are possibly subserved by frontoparietal regions, we believe that the claims of

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Binder et al. (2017) require further discussion. In particular, we believe that the pattern of results

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from the study highlights the possible contribution of body-centered spatial representations or

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kinematics in apraxia, beside that of action simulation mechanisms, and that these functions may

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also be associated with proposed mirror regions. We aim to make this distinction clear in order to

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stimulate a deeper understanding of the possible role for the putative human MNS for higher-order

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action understanding and perception.

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Though Binder et al. (2017) claim that “lesions to the core regions of the putative hMNS

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critically affected key functions ascribed to it” (p. 135), simulative mechanisms are by no means the

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only essential component of these functions, as has been noted by others (Buxbaum & Kalénine,

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2010). Similarly, mirror mechanisms are not the only process associated with proposed mirror

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regions such as the left inferior parietal lobule (IPL). To expand on this point, Binder et al. (2017)

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found that apraxia patients were also significantly worse than non-apraxic patients and healthy

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controls in the gesture recognition control task (testing the ability to evaluate the spatial distance

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between the model’s hand and head). They suggest that the significant effect in this task could be

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due to proposed left hemisphere apraxia deficits in ‘body part coding’ (Goldenberg & Karnath,

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2006). This approach to apraxia suggests that the observed deficits can be considered a problem of

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correctly assessing the spatial relationship between body parts (such as the hand) and other body

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parts or objects. Thus, they interpret their results in the recognition control task by suggesting that

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the coding of spatial relationships between body parts may have been impaired in their apraxic

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patients. However, this may also provide an explanation for the other results observed in this

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experiment, since an inability to accurately assess the spatial relationships between body parts in

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different gestures could feasibly make recognition, comprehension, and imitation harder to

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complete. Unfortunately, the authors do not report whether any lesioned areas were associated with

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this control task and whether these overlapped with the reported regions predicting the impairments

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in the experimental tasks.

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Notable in Binder and colleague’s (2017) study is the anterior-posterior split between lesions

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associated with gesture comprehension (anterior) and lesions associated with gesture imitation

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(posterior). Previous evidence does seem to support a vital role for the left IFG in action

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understanding (Urgesi et al., 2014), which could be associated with the proposed simulative role of

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mirror neurons. However, there may be a different explanation for the role of posterior regions in

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imitation. A VLSM study by Buxbaum et al. (2014) suggests that left IPL damage is associated with

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deficits in the kinematic aspects of imitation, whereas damage to the posterior temporal lobe is

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associated with deficits in the postural aspects of imitation. Similar results were reported more

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recently by Dressing et al. (2016). Since Binder et al. (2017) did not distinguish between the

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kinematic and postural elements of their imitation task during analysis, it is unclear to what degree

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these different elements of movement might better explain their results. Discussion on these terms

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may better account for the fact that left parietal lesions frequently cause deficits in the imitation of

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novel actions (Goldenberg, 2009). Since mirror approaches to social cognition rely on the idea that

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mirror neurons are involved in visuomotor matching of observed and stored actions (Rizzolatti et

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al., 2014), it is yet unclear how visuomotor matching is a feasible explanation for defective

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imitation of novel actions, since there should be no stored action representation to match. On the

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other hand, both novel and known actions could be coded in terms of the observed postural or

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kinematic parameters, with novel actions showing a greater reliance on this type of information

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(Rumiati et al., 2009; Rumiati & Tessari, 2002; Tessari & Rumiati, 2004). It is possible then that in

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this instance the anterior-posterior split does not necessarily reflect two mirror mechanisms, but

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rather a distinction between simulative and spatial or kinematic mechanisms for social motor

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behaviour.

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Finally, we are in agreement with Binder et al. (2017) when they state that the “lack of

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significant result for the VLSM of our Gesture Recognition task is in line with [the claim] that in

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contrast to gesture comprehension a mere recognition of correctly performed familiar gestures is not

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a core function of the human MNS” (p. 134). In fact, action recognition could be principally

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subserved by occipitotemporal regions (Lingnau & Downing, 2015; Peelen & Downing, 2017), as

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recent evidence suggests that visual representations of body parts and action in this area are

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organised in terms of semantics, transitivity, and sociality (Bracci et al., 2015; Wurm et al., 2017),

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and that the structure of these representations could possibly assist in higher-level social cognition

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in a bottom-up manner (Reader, 2016). Previous VLSM approaches to deficits in gesture

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recognition, particularly for semantic aspects of action, reflect the importance of these regions

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(Kalénine et al., 2010).

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In conclusion, whilst Binder et al. (2017) confirm the role of frontoparietal regions in

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apraxia, there is still much work to be done to fully understand the contribution of these areas to

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both apraxia and social motor behaviour as a whole. Importantly, deficits following damage to

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proposed regions of the human mirror network can also provide support for proposed functions of

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these regions apart from a mirror mechanism. In social interaction we believe it is fundamental to

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understand the contribution of regions coding for the kinematic, spatial, or postural features of

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action, over a purely mirror neuron driven approach.

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