Neural correlates of manual action language: Comparative review, ALE meta-analysis and ROI meta-analysis
Introduction
The cerebral network of action language has been the focus of extensive research in the last decades and a wide range of theories on language embodiment have been developed (e.g. Binder and Desai, 2011; Gallese and Lakoff, 2005; Glenberg, 2015; Mahon and Caramazza, 2008; Pulvermüller, 2013; Zwaan, 2014). However, the specific role of the motor system in action language processing and the extent to which action language is embodied remain controversial (Meteyard et al., 2012; Zwaan, 2014). Functional magnetic resonance imaging (fMRI) studies have played an important part in demonstrating the involvement of the motor system during the processing of action language (e.g.Hauk et al., 2004; Kemmerer et al., 2008; Labruna et al., 2011; van Dam et al., 2012). Evidence has accumulated that suggests that the relationship between action language and the motor system varies as a function of several factors, including context, expertise, attentional focus and semantic control demand (Davey, 2015; Moody and Gennari, 2010; Yang, 2014; Zwaan, 2014). This suggests that the involvement of the motor system in action language processing is complex but important questions remain. What is the nature of this motor involvement? What are the motor-related neural mechanisms at play during action language? Of particular interest are the studies that directly compared action language with other motor-related processes. Such comparisons have revealed similarities between the action language network and the networks of motor observation (Aziz-Zadeh et al., 2006; Meister and Iacoboni, 2007), motor imagery (Yang and Shu, 2014) and motor execution (Moody-Triantis et al., 2014; Papeo et al., 2012; Peck et al., 2009). However, a lack of overlap between the neural networks of action language and these other motor-related processes has also been reported (Tomasino et al., 2007; Tremblay and Small, 2011; Willems et al., 2009; Zhang et al., 2018). Thus, agreement about the relationship between the neural networks supporting action language processing and those supporting other motor-related processes has not been reached yet.
Meta-analyses provide a quantitative methodology to summarize empirical data, which may help in reaching a consensus. Meta-analyses have been conducted to characterize the cerebral network of action language (Jirak et al., 2010), motor observation (Caspers et al., 2010) and motor imagery (Hétu et al., 2013), providing a comprehensive overview of the neural networks involved in each of these processes. A more recent meta-analysis compared motor observation, imagery, and execution (Hardwick et al., 2018) and revealed that motor execution shared more activation sites with motor imagery than with motor observation. A systematic meta-analysis comparing action language, motor observation, imagery, and execution would provide unique and important insights into the motor processes involved in action language processing.
The main objective of the present study was to provide a comprehensive analysis of the fMRI literature on action language processing and its links with other motor-related processes (motor observation, imagery, and execution) through a systematic review of the literature and a two-fold meta-analysis (ALE and ROI). The aims of the systematic review were to generate a clear portrait of research on the neural correlates of action language processing and to examine whether this literature has explored action/movement-related parameters that have been explored in other motor-related fields of research. The overall aim of the ALE meta-analysis was to characterize the motor-related network of action language processing in comparison to those of motor observation, imagery, and execution. The first specific objective was to compare action language, motor observation, and motor imagery to motor execution in order to confirm the existence of a gradation in the similarity of the neural networks associated with these processes to the motor execution network. Considering that the motor execution network is more similar to the network of motor imagery than motor observation (Hardwick et al., 2018), and that the network of action language is more similar to motor observation than execution (Rueschemeyer et al., 2014), we expected action language to be the least “motoric” of the following motor-related processes on a motor gradation: motor execution – motor imagery – motor observation – action language. The second specific objective was to determine to which motor-related process the action language network was most similar. Since the action language network has been shown to be more similar to motor observation than to motor execution (Rueschemeyer et al., 2014), we expected the degree of similarity between action language and other motor-related processes to follow the previously mentioned motor gradation: the neural network of action language would be more similar to that of motor observation, then to motor imagery and finally to motor execution. The third specific objective was to determine whether the action language network was more closely related to movement or action processing. We hypothesized that the action language network would be more similar to the action compared to the movement processing network. Finally, an anatomical ROI meta-analysis aimed to provide complementary information regarding the functional network for action language by comparing, region by region, the bilateral language activation to the profile for motor imagery, observation, and execution.
Section snippets
Search strategy
Four comprehensive electronic literature searches were performed using PubMed in January 2018 and updated in March 2019. The searches separately identified studies focusing on manual action language, motor observation, imagery, and execution. The following key search terms (in all fields) included: (1) (action language OR action verbs OR embodied language) AND (hand OR manual OR finger) AND fMRI, (2) action observation2
Meta-analysis
The general objective of the meta-analysis was to characterize the brain networks involved in action language processing and to compare these networks to those of motor observation, imagery, and execution as a way to gain further knowledge about the mechanisms involved in action language processing. The analysis was divided into two components: a series of activation likelihood estimation (ALE) analyses and an anatomical region of interest (ROI) analysis. The ALE analyses allowed for the direct
Discussion
The general objective of this study was to provide a systematic and statistically supported account of the state of research on the neural correlates of action language processing. To this aim, a systematic review of the literature and two kinds of meta-analyses were conducted (ALE and ROI-based). Four main findings emerged: (1) the motor parameters that are frequently considered in motor observation, imagery, and execution studies are rarely considered in action language research, (2) there is
Conclusion
The present research is the first to compare the functional network of action language to those of motor observation, imagery, and execution using three different approaches: a systematic review of the literature, an ALE whole-brain meta-analysis and a ROI-based meta-analysis. The review of the literature highlighted the experimental standards in research on motor observation, imagery, and execution, that action language research needs to adopt if bridges are to be built across research fields.
Acknowledgements
This study was supported by a grant from the Canadian foundation for innovation to P.T. (31408), who also holds a Career Awards from the “Fonds de Recherche du Québec – Santé’’ (FRQS; 35016).
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Present address: Département de neurosciences, Université de Montréal, Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal, 4545 chemin Queen-Mary, H3W 1W4, Montreal, QC, Canada.