Learning via imitation and through the internal representation of movement is thought to be one of our primary modalities of
learning and consolidating new motor skills. The mirror neuron system (MNS) is a fronto-parietal network of multimodal neurons in
the central nervous system that has an integrative role in these processes, firing when a person observes, imagines, executes, and
imitates actions (Decety, 1996; Iacoboni & Dapretto, 2006). This network has recently been hypothesised to contribute to the motor
impairments that are characteristic of developmental coordination disorder (DCD) (Licari et al., 2015; Reynolds, Licari, Billington
et al., 2015; Reynolds, Thornton et al., 2015; Werner, Cermak, & Aziz-Zadeh, 2012). Deficits in imitation (Elbasan, Kayıhan, &
Duzgun, 2012; Reynolds, Kerrigan, Elliott, Lay, & Licari, 2016; Sinani, Sugden, & Hill, 2011; Zoia, Pelamatti, Cuttini, Casotto, &
Scabar, 2002) and motor imagery performance (Adams, Lust, Wilson, & Steenbergen, 2014; Reynolds, Licari, Elliott, Lay, & Williams,
2015) in children with DCD have been used to support this hypothesis. To extend our knowledge of this system, further research is
required to increase our understanding of the functioning of this system at a neurological level (Reynolds, Licari, Billington et al.,
2015; Reynolds, Thornton et al., 2015). Functional activation differences in mirror neuron regions may underlie the motor, imitation,
and motor imagery impairments, and contribute to the movement difficulties characteristic of children with DCD.
The MNS circuit in humans is believed to incorporate the pars opercularis (BA44) of the inferior frontal gyrus (IFG; Kilner, Friston,
& Frith, 2007), the adjacent ventral premotor cortex (PMv; BA6; Buccino et al., 2001; Grafton et al., 1996; Rizzolatti et al., 1996) and
the rostral inferior parietal lobule (IPL; BA 39 and 40; Arbib, Billard, Iacoboni, & Oztop, 2000; Caspers, Zilles, Laird, & Eickhoff, 2010;
Rizzolatti & Craighero, 2004; Fig. 1). These mirror regions fire when one actively observes, imagines, executes, or imitates a
movement, with a progressive increase in functional MRI (fMRI) blood-oxygen-level dependent (BOLD) signal from observation
through to imitation (Aziz-Zadeh, Koski, Zaidel, Mazziotta, & Iacoboni, 2006). Another important area involved in the MNS is the
superior temporal sulcus (STS). Although STS neurons are not activated during motor execution (Aziz-Zadeh, Koski et al., 2006;
Buccino, Solodkin, & Small, 2006), this area is thought to be connected with mirror regions via the arcuate fasciculus and parallel
tracts (Catani, Jones, & ffytche, 2005; Iacoboni et al., 1999; Rizzolatti et al., 2001) and is believed to play an important role in visual
input during observation by coding for goal-directed and meaningful actions (Jellema, Baker, Wicker, & Perrett, 2000; Perrett et al.,
1989). The human MNS has been proposed to represent a ‘dynamic feedback control system’ (Schippers & Keysers, 2011, p. 40) that
supports both forward and inverse internal modelling processes, with a primary predictive control function (Fig. 1).
Fig. 1. Information flow in the mirror neuron system (STS: superior temporal sulcus, IPL: inferior parietal lobule, PMv: ventral premotor cortex, IFG: inferior frontal
gyrus; (created using images from BrainVoyager Brain Tutor: http://www.brainvoyager.com/products/braintutor.html; Goebel, Esposito, & Formisano, 2006).
J.E. Reynolds et al. Research in Developmental Disabilities 84 (2019) 16–27
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At a behavioural level, research exploring deficits in imitation and motor imagery performance has been used as evidence to
support the MNS dysfunction hypothesis of DCD (Reynolds, Thornton et al., 2015; Werner et al., 2012). Imitation provides a
foundation for skill learning via observation and is an important mechanism from a young age (Arbib et al., 2000; Billard & Arbib,
2002). The use of motor imagery, on its own, and in conjunction with traditional motor execution training, has repeatedly been
shown to improve motor skill performance (Buccino et al., 2006) and assist motor skill development and acquisition (Decety, 1996).
Imitation of learned, meaningful skills (Dewey, 1993; Sinani et al., 2011; Zoia et al., 2002) and non-meaningful simple and complex
gestures (Elbasan et al., 2012; Goyen et al., 2011; Reynolds et al., 2016) have been shown to be performed poorly by children with
DCD, who make more errors and respond slower to visual cues. In addition to imitation deficits, children with DCD have difficulty
with motor imagery. Results on mental rotation and other motor imagery tasks suggest that children with DCD are able to adopt the
use of a motor imagery strategy; however, they make slower, less accurate responses to stimuli (Adams et al., 2014, 2017; Fuelscher
et al., 2016; Reynolds, Thornton et al., 2015).
In addition to the behavioural evidence, some support for MNS dysfunction is evident in the small body of fMRI research in this
population (Debrabant, Gheysen, Caeyenberghs, Van Waelvelde, & Vingerhoets, 2013; Kashiwagi, Iwaki, Narumi, Tamai, & Suzuki,
2009; Licari et al., 2015; Zwicker, Missiuna, Harris, & Boyd, 2010, Zwicker, Missiuna, Harris, & Boyd, 2011). Although not directly
exploring MNS function, these studies have identified differences in activation patterns, and functional (McLeod, Langevin,
Goodyear, & Dewey, 2014, McLeod, Langevin, & Dewey Goodyear, 2016) and effective (Querne et al., 2008) connectivity of cortical
areas linked to the MNS, using a range of tasks and resting state paradigms. The strongest initial evidence for possible MNS dysfunction
comes from a recent fMRI study conducted by Licari et al. (2015), who found that during the imitation of a finger sequence
task, children with DCD had decreased activation in the left IFG compared to controls. Hypothesised to possibly reflect MNS dysfunction,
a follow up study was undertaken to specifically explore MNS functioning during observation, execution, and imitation of
the same finger sequencing task (Reynolds, Licari, Billington et al., 2015). The control group was found to have significantly greater
activation than the DCD group during observation in the pars opercularis of the IFG, the precentral gyrus, middle temporal gyrus,
posterior cingulate, and precuneus (Reynolds, Licari, Billington et al., 2015). In addition, an interaction effect between group and
task condition was seen in the pars opercularis, a key MNS region, with the DCD group showing a large deactivation in this region
during imitation compared to the other conditions (Reynolds, Licari, Billington et al., 2015). Although suggested to provide preliminary
evidence for MNS dysfunction, and children with DCD possibly adopting different neural strategies while performing the
different task conditions, the lack of expected MNS signal increase from execution to imitation at a whole brain level was interpreted
as a potential learning effect, whereby the extent of activation of MNS regions was likely reduced, which may have prevented group
differences during execution and imitation from being identified.
Further research to explore hypothesised MNS dysfunction using simple target-directed finger movements without practice prior
to scanning to circumvent the possible effect of motor learning, and to incorporate motor imagery into the fMRI task paradigm is
required (Reynolds, Licari, Billington et al., 2015). Therefore, the present study aimed to use fMRI to investigate whether a deficit in
the MNS exists in children with DCD by examining brain activations during the performance of a target-directed adduction/abduction
finger tapping task (modified from: Aziz-Zadeh, Koski et al., 2006; Aziz-Zadeh, Maeda, Zaidel, Mazziotta, & Iacoboni, 2002) under
four conditions: (1) action observation; (2) motor imagery; (3) action execution; and (4) imitation. (Aziz-Zadeh, Koski et al., 2006;
Decety, 1996; Iacoboni et al., 1999). It was hypothesised that there would be decreased activation in the MNS of children with DCD
compared to controls, specifically in the pars opercularis of the IFG, the PMv, IPL and STS, most prominent during the imitation
condition. In addition, this study also aimed to explore other cortical areas that may contribute to the movement difficulties seen in
children with DCD.
