Motor Simulation

Motor simulation can be defined as the internal representation of a motor programme without any overt actions (Jeannerod, 2001). It has two major modalities: motor imagery (MI), which is defined as imagining the execution of an action without any physical output, and action observation (AO) which means watching others performing actions. MI can be divided into two different modalities: visual imagery (VI) and kinaesthetic imagery (KI) (Guillot et al., 2009). VI involves the self-generation of actions from a first (internal VI) or third (external VI) person perspective. During the first person perspective (IVI), people visualise the action as it would happen in real-life, and see images ‘as if through their own eyes’. During external visual

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imagery (EVI), people imagine, like spectators, the action that somebody is performing. In contrast, KI includes the sensations of how it feels to perform an action, including the force and effort perceived during movement. This can only be experienced with an IVI (Vogt et al., 2013). A large body of research has examined the advantages of MI in aiding elite athletic performance (Williams et al., 2015), improving motor ability in healthy and clinical populations (for review see: Schuster et al., 2011), skill acquisition (Lotze and Halsband, 2006) and rehabilitation (Ietswaart et al., 2011). Similarly, AO has gained increasing attention since early 2000s following the discovery of the mirror neuron system (MNS) in monkeys (Gallese

et al., 1996; Rizzolatti et al., 1996) and in humans (Fabbri-Destro and Rizzolatti, 2008). Mirror

neurons fire both when an action is physically performed and when it is being observed. AO plays an important role in motor learning through imitation (Buccino et al., 2004) and has been used in neurorehabilitation (Buccino, 2014) and in consolidation of motor memories (Zhang et

al., 2011).

An activation likelihood estimation (ALE) analysis highlighted that MI and AO recruit motor and motor related regions which overlap extensively with one another, and overlap with the regions involved in motor execution (ME) (Caspers et al., 2010; Hétu et al., 2013; Hardwick et al., 2017). The conjunction analysis across MI, AO and ME has identified a consistent activation in the fronto-parietal motor network, in areas including:

 Premotor Cortex (PM): A bilateral ventral premotor (vPM), dorsal premotor (dPM) and supplementary motor area (SMA) shown to be consistently involved during MI, AO, and ME. The PM plays important roles in the planning, preparation and execution of actions (Hoshi et al., 2007). Imagined and executed actions require almost the same amount of time to be performed, suggesting that MI also includes planning and preparation phases with an inhibitory execution (Guillot and Collet, 2017). vPM is believed to play a major role in fine motor coordination (Davare et al., 2009), while

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dPM has a limited contribution towards movement execution (Dum and Strick, 2005), and therefore is proposed to play a role in action selection (Rushworth et al., 1998). SMA is the medial region of the PM, and it is associated with linking conditional roles with actions (i.e. where an action A is performed by a condition B) (Nachev et al., 2008), and internally initiated movements that require sequences of actions (Nachev et

al., 2007; Hoffstaedter et al., 2013).

 Primary Motor Cortex (M1): The involvement of M1 in action simulation is controversial. Caspers et al., (2010) found evidence that M1 may only be recruited during action observation when participants view actions with the intention to imitate them. Similarly, Hétu et al., (2013) found no evidence of consistent recruitment of M1 during motor imagery, and Hardwick et al. (2017) found consistent involvement of M1 only during ME. Jeannerod (2001) reported that M1 activation during MI and AO was less than during ME, suggesting that M1 may be active at a different, lower level, which is not sufficient to induce a local maxima (Lotze and Halsband, 2006).

 Somatosensory Cortex: The involvement of the somatosensory cortex during MI reflects kinaesthetic aspects of motor imagery, while in AO, its recruitment is proposed to extend the mirror properties beyond the motor system (Keysers and Gazzola, 2009). In ME, sensory input provides critical feedback for the accuracy of the movements, allowing comparison between the actual and expected sensory consequences of movements (Muckli and Petro, 2017).

 Parietal Cortex: The parietal cortex is an important multisensory hub involved in processing visuomotor information for the online control of movements, guided by a visual input (Block et al., 2013). In Block et al (2013), the bilateral inferior parietal lobule region (IPL) was consistently activated across all modalities. IPL is involved in various cognitive functions, such as the processing of tactile information (Klann et al.,

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2015) and storing several motor representations that are organised somatotopically (Cooke et al., 2003; Rozzi et al., 2008). The involvement of IPL reflects the interaction between the parietal and premotor cortices during visumotor control of motor functions, and the internal recruitment of these motor representations (Wise et al., 1997).

Although distinct brain structures are identifiable for AO, MI and ME individually (Lorey et al., 2013; Filimon et al., 2015), the ALE analysis identified that a wide network of regions were active during both MI and ME, including the cerebellum, basal ganglia, and mid- cingulate cortex (Hardwick et al., 2017). The cerebellum contains multiple representations of the body, and Lobule VI contains body representations that are most prominent during movement execution (Schlerf et al., 2010). The basal ganglia are associated with response selection and speed of imagined and executed actions. Both MI and ME recruited regions of mid-cingulate cortex that are proposed to play a role in movement production.

While the majority of previous research has focused on MI or AO as independent approaches, or on the similarities and differences between these two forms of motor simulation, there is now an emerging body of research showing the potential advantages for MI guided by AO (AO+MI) (Vogt et al., 2013; Eaves et al., 2016). AO+MI involves imagining the physiological sensations and kinaesthetic experiences of actions (MI task), and synchronising these with the congruent observed action (AO task). Combining these two modalities into one (AO+MI) could engage more of the frontal-parietal network than is involved in ME, and give greater control over the content and vividness of action simulation (Holmes and Calmels, 2008). Few studies have examined the recruited cortical brain regions during AO+MI, MI and AO (for review see (Eaves et al., 2016)). Macuga & Frey (2012) reported that brain regions recruited in AO are a subset of those involved in AO+MI, which in turn are a subset of those involved in imitation. Nedelko et al. (2012) and Villiger et al., (2013) also reported that AO+MI increased neural activity over the AO in parts of the cerebellum, inferior frontal gyrus, inferior

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parietal cortex, SMA, vPM and left insula. Taube et al. (2015) showed that AO+MI had a greater neural activity in the caudal supplementary motor area (SMA), basal ganglia, and cerebellum compared to AO; and in the bilateral cerebellum and precuneous compared to MI. AO+MI has been used as a tool to improve performance in a golf putting task (Smith and Holmes, 2004) and a bicep curl strength test (Wright and Smith, 2017) over 6 weeks of intervention. Clinically, AO+MI has been used in rehabilitation programs, but it has shown a mixed effect. Small scale studies have targeted stroke patients with upper limb motor dysfunction, and these have provided promising results in terms of improvement in motor functions over 4 weeks intervention (Ertelt et al., 2007; Sun et al., 2016). However, Ietswaart et al. (2011) reported that AO+MI intervention did not enhance motor recovery of stroke patients with persistent upper limb motor weakness. An interesting next step could now involve a more in-depth examination into the precise anatomical substrates involved in different AO+MI tasks, using multivariate pattern analysis (MVPA) of fMRI data.