A surprising finding in contemporary neuroscience concerns the motor system’s function as a vehicle for higher cognitive processes which, on first glance, appear to be entirely unrelated to basic motor function. Theoretical bridges between supposedly “lower-order” sensorimotor functions and cognitive processes, such as developing semantic concepts or language, have been proposed in the psychological literature (Piaget, 1950). Recent research indicates that this link may lie in action-perception circuits, neuronal ensembles connecting neurons in sensory and motor areas via brain systems intertwining the two (Pulvermüller, 1999; Fuster, 2003; Rizzolatti and Craighero, 2004; Jeannerod, 2006; Pulvermüller and Fadiga, 2010). Correlated activation in motor and sensory areas of the cortex is proposed to lead to the development of neuronal assemblies that represent motor acts. These action-perception circuits become the basis of mirroring, i.e., repeating visually perceived actions performed by others, repeating verbal utterances and working memory (Fuster, 2003; Rizzolatti and Craighero, 2004; Jeannerod, 2006).

Critically, however, by interlinking with each other, such action-perception circuits can themselves become substrates for a range of additional higher cognitive processes, such as language and representation of conceptual meaning. Words denoting concrete, visible concepts, such as actions or visible objects, tend to be learnt in the context of interacting with or experiencing that concept in the world (Pulvermüller, 1999). In accordance with Hebbian principles, simultaneous activation across numerous brain regions results in the formation of connected circuits. Specifically, the sensorimotor patterns for hearing and articulating a word (represented in core perisylvian language areas, Figure 1A) become linked to the differential areas activated by experiencing/interacting with actions or objects, thus forming conceptual circuits for words. Action words such as “grasp,” which semantically relate to the concepts of actions represented by action schemas stored in cortical motor systems, therefore draw upon motor systems, whilst object words relate to visual objects and are thus processed in the temporo-occipital visual processing stream. This is depicted in Figure 1B, (but please see Garaghani et al., 2009 for elaboration on this model and the linkage of regions through Hebbian processes). Though this relates to concrete items, there may be a critical role for action-perception circuits in the representation of meaning for abstract words, too (Moseley et al., 2012). In addition, elementary action schemas can be linked into action chains and may multiply into action hierarchies, thus embedding actions and object representations into plans and frames (Pulvermüller and Fadiga, 2010). Research in social neuroscience has also repeatedly shown that action-perception systems involved in mirroring can interact synergistically with mentalizing systems (Zaki et al., 2009; Lombardo et al., 2010a; Schippers et al., 2010; Spunt and Lieberman, 2012). This mutual link suggests that motor problems may lead developmentally to a whole host of downstream deficits in higher cognitive functions (e.g., language, communication, social cognition, understanding action concepts, and the meaning of action words; Pulvermüller, 2005; see Figure 1).

If action-perception circuits form one basis of higher cognition, a motor deficit could hinder their formation and thus compromise, or alter, higher processes normally built upon the latter. Critical test cases here are patients with motor impairments, such as in stroke, Parkinson’s disease, or Motor Neuron disease, who indeed show specific deficits in understanding action-related concepts and in processing action-related words (Neininger and Pulvermüller, 2003; Boulenger et al., 2008; Bak and Chandran, 2011; Kemmerer et al., 2012). On this basis, it is however difficult to confidently attribute the motor systems a critical role in cognition: lesions are typically characterized by substantial involvement of multiple regions which limits linkage of cognitive deficits to this focal area. A syndrome marked by more subtle motor deficits and a broad range of social and cognitive difficulties may allow testing of new predictions regarding the role of sensorimotor systems in higher cognitive processing and corroborate the evidence provided by other neuropsychological patient groups, especially if behavioral experiments are combined with spatially precise neuroimaging.

A case in kind are autism spectrum conditions (ASC), neurodevelopmental conditions primarily diagnosed by the “triad” of social-communication deficits, stereotyped/repetitive behaviors, and unusually restricted/narrow interests. Interestingly, ASC are also commonly characterized by subtle motor impairments in gait, posture, fine and sometimes gross coordination (Jansiewicz et al., 2006; Dewey et al., 2007; Dziuk et al., 2007). Perhaps due to the somewhat hidden nature of any potential link between social-communicative deficits and non-social motor abnormalities, the latter have traditionally been seen as minor, secondary phenomena, especially as the social-communicative deficits of autism are far more disabling. Emerging evidence, however, supports the idea that sensorimotor abnormalities precede the emergence of core social-communicative problems in infants at risk for developing autism (Teitelbaum et al., 1998; Rogers, 2009) and that later deficits in social interaction, imitation, and social cognition may emerge downstream from the atypical development of sensorimotor systems (Mostofsky et al., 2006). A further hint that socio-cognitive deficits and motor processes are linked comes from the mirror neuron literature, where inferior frontal and premotor “mirror neuron systems” (MNS) are hypoactive in ASC [Iacoboni and Dapretto, 2006; Cattaneo et al., 2007; Williams, 2008; Rizzolatti and Fabbri-Destro, 2010; though the role of the mirror system in autism is debated by other authors (Marsh and Hamilton, 2011)]. If a motor deficit precedes or is intertwined with higher cognitive deficits in ASC (Leary and Hill, 1996), the investigation of motor brain mechanisms, conceptual action understanding and severity of ASC may be fruitful in understanding the mechanisms of these complex conditions.

Dysfunction of action-perception circuits in ASC implies that these individuals should fail to activate action representations in speech comprehension, especially during understanding of action-related meanings (Figure 1). In contrast, when typically developing (TD) participants read action words or sentences, motor activation reflects somatotopic aspects of word meaning (Hauk et al., 2004; Pulvermüller and Fadiga, 2010). If action-perception circuits are indeed a basis for understanding action-related language, a further prediction is that people with ASC should exhibit a specific deficit in semantically understanding action words. Crucially, behavioral and motor-cognitive brain activation deficits should correlate with and should predict autistic traits.

To test these predictions of the action-perception model, we used event-related fMRI to assess patterns of cortical activation during passive reading and comprehension of action and object words in individuals with ASC and TD controls, and carried out a behavioral experiment to assess their ability to semantically classify these words. To elucidate links across different levels of brain and behavior, we then investigated correlations between motor system activation and cognitive-semantic ability, and also the correlation between activation and the number of autistic traits as measured by the Autism Spectrum Quotient (AQ; Baron-Cohen et al., 2001). Employing a data-driven regions of interest (ROI) approach, we were able to investigate activation evoked by action- and object-related words in frontal and temporal areas typically involved in language (Pulvermüller, 1999; Cohen et al., 2002; Kronbichler et al., 2004) and regions in the motor system which typically respond to action words (Pulvermüller and Fadiga, 2010). Given the movement impairments and structural abnormalities of motor systems in ASC, we hypothesised that these individuals would show a category-specific abnormality during the processing of words with action meaning. If motor systems play an important role in retrieving the meaning of action words, a processing deficit for these words manifested in psycholinguistic semantic tasks should be predicted by abnormal activity for action words in this motor region.

Here we report a novel investigation of semantic action word processing in ASC and its relationship to motor cortex activation and general ASC symptomatology. Using fMRI, we found hypoactivation of inferior-frontal and premotor cortex during word reading in ASC relative to matched control participants. This reduction in activity was most clearly apparent for words semantically related to actions. Corresponding to the significantly reduced activation of motor systems in action word processing seen in ASC, we found increased reaction times for processing these words in this group, thus indicating a category-specific abnormality in semantic processing. Third, linking the two results together, a significant correlation emerged between hypoactivity in the motor system and slowed reaction time for processing action words. Critically, a similar correlation also appeared between semantic hypoactivity and autistic symptomatology in our ASC group. These results all support the prediction of an action-perception theory of ASC, whereby the reported category-specific semantic processing disadvantage, and possibly a wider range of ASC symptoms, may stem from atypical information exchange between the motor cortex and other brain regions.

This newly observed language-related hypoactivation of motor systems in ASC and their correlated deficit in semantically processing action-related words refute an interpretation of semantic motor systems activation as “ancillary” or “epiphenomenal” in the general population. Rather, it appears that an intact and well-connected motor system brings about motor system activation during action word reading and is necessary for optimal processing of these items, whereas, in a condition where this activation is absent, specific abnormalities in semantic information processing are manifest for words with action-related meaning. “Disembodied” theories of conceptual representation (Mahon and Caramazza, 2008), assuming meaning processing divorced from sensorimotor systems, cannot account for this finding. Nor is there currently evidence to suggest the activation of motor systems by another region or system (see Kiefer and Pulvermüller, 2012, for review and discussion of the literature). Although a range of cortical areas take their share in meaning processing (Pulvermüller, 2013), the present study failed to reveal brain activation outside the motor system that predicted the ASC-specific deficit in semantic processing of action-related words.

To account for the observed correlations between motor system hypoactivity, action-semantic deficit and ASC symptomatology, parsimony demands that a causal link be postulated. That socio-communicative or semantic deficits in autism might give rise to motor impairments seems unlikely, given that such a proposition would fail to explain why semantic deficits are specific to action words or why premotor cortex is hypoactive in language processing; furthermore, this position seems difficult to reconcile with the early emergence of motor dysfunction in ASC, long before semantic or social deficits become manifest or at least evident to current means of measurement at this age (Teitelbaum et al., 1998; Rogers, 2009). As there is currently no evidence for a third process acting on both motor and semantic systems, the third possibility is offered by action-perception theory. A functional deficit in motor areas and/or in the interaction between motor and other brain systems (see Figure 1), leads to atypical development of action-perception circuits required for language processing, motor cognition and action semantics. Thus the ASC motor deficit, which emerges early in ontogenesis, would cause hypoactivity in the precentral cortex in action-semantic processing and the observed slowing of action-semantic classification in ASC. On the basis of the existing literature on ASC and the specificity of the present results, such an account is highly plausible.

The observed action-semantic deficits in autism are paralleled in patients suffering from lesions in the motor system (Neininger and Pulvermüller, 2003; Boulenger et al., 2008; Bak and Chandran, 2011). The significant advance of the present study is the specificity of the relationship between cognitive-semantic deficits and the functionality of focal precentral cortex activation. The functional importance of motor systems for higher cognition demonstrated by earlier cognitive and brain research (Buccino et al., 2005; Pulvermüller et al., 2005; Fischer and Zwaan, 2008; Shebani and Pulvermüller, 2013) fits with a potential causal role of autistic motor dysfunction, as suggested by the developmental primacy of motor symptoms relative to core autistic symptomatology (Teitelbaum et al., 1998; Rogers, 2009). Indeed, impairments in the motor system in ASC and its connectivity predict not only movement problems but difficulty establishing typical action-perception circuits and therefore representations of complex actions (Mostofsky and Ewen, 2011). In turn, such representational alteration may lead to higher-order deficits in action understanding (Blake et al., 2003; Williams, 2008), gesture and imitation (Williams et al., 2001; Dewey et al., 2007), as well as language and communication. Although presently unascertained, it appears plausible that the aberrant structural connectivity of cortico-cortical tracts and reduced functional connectivity in ASC (Courchesne and Pierce, 2005; Sundaram et al., 2008; Jones et al., 2010) contribute to their motor and cognitive impairments. Atypical connectivity between frontal action-systems and posterior perception-related neural systems in the arcuate fascicles, which connect anterior and posterior language regions (Keller et al., 2007; Fletcher et al., 2010; Lai et al., 2012), may be of special relevance here, considering the key role these pathways play in connecting action-perception circuits, thus merging information about actions and perceptions in linguistic and semantic neural systems (Pulvermüller and Fadiga, 2010). The atypical development of language circuits would explain why, during reading words of different semantic categories, participants with ASC exhibit atypical patterns of local cortical activity (Moseley et al., 2013). We were unable, in the present study, to ascertain the degree of cortical motor abnormality in our participants, and this, alongside perhaps the course-grained measure of semantic processing in our behavioral task, might explain why inaccuracy in action word processing was not revealed alongside longer reaction times. The “tipping point” at which brain abnormalities manifest in semantic errors is likely to be influenced by task demands. It is clear that this study convincingly supports the contribution of motor regions to optimal action word processing, but much remains to be elucidated regarding the contribution of these and other brain areas to semantic processing in different contexts (Hauk and Tschentscher, 2013; Pulvermüller, 2013).

Action-perception circuits provide a functional link between sensory and motor neurons and become active when the individual performs an action and when they perceive the action visually or hear its characteristic action sounds (see Figure 1B). This mechanism explains the response patterns of mirror neurons, which play a key role in these circuits. Over and above providing a mechanism of mirror neuron activity and behavioral imitation, these action perception circuits can support a range of higher mental processes necessary for language, semantics, and social cognition (Pulvermüller and Fadiga, 2010). The lack of “embodied” action-related semantic processing in ASC demonstrated for the first time in this study is therefore in agreement with the well-known inactivity of the mirror neuron system seen in ASC subjects during tasks unrelated to language (Iacoboni and Dapretto, 2006; Cattaneo et al., 2007; Williams, 2008; Rizzolatti and Fabbri-Destro, 2010). In this context, the correlation between language-evoked motor activation and autistic traits (AQ scores) bolsters the previous suggestion that a range of typical ASC symptoms relate to motor systems abnormalities (Mostofsky et al., 2006; Mostofsky and Ewen, 2011). Although our present data are consistent with the prediction that an impairment of mirror mechanisms relying on action perception circuits would entail ASC deficits in semantic motor system activation, semantic processing of action words, and even general traits of ASC, we hasten to emphasize that that our data are correlational and therefore cannot provide proof of causality. Still, we offer some related considerations in the following paragraph.

Atypical grounding of semantics in action-perception circuits, such as would result in abnormal linguistic/communicative processing, might derail further development in domains that depend on input from motor systems, such as mentalizing. In particular, several researchers have hypothesized that “embodied” premotor cortical systems involved in mirroring also interact with systems for mentalizing (Zaki et al., 2009; Lombardo et al., 2010a; Schippers et al., 2010; Spunt and Lieberman, 2012). For example, reduced functional connectivity in ASC has been observed between a key mentalizing/self-representation region, ventromedial prefrontal cortex, and ventral premotor cortex and somatosensory cortex (Lombardo et al., 2010b). This would suggest that atypical development of (premotor-prefrontal links in) action-perception circuits underlying higher cognition could impact on the way in which individuals with ASC interact with others (Lombardo and Baron-Cohen, 2010,2011), and how such motor problems, preceding higher-level socio-communicative difficulties, might set children on atypical trajectories that lead to increased risk for autism. Though implications beyond the semantic processes studied in this present work may appear as speculative, our results clearly demonstrate that motor problems in ASC cannot be regarded as separate from, or secondary to, higher cognitive and socio-communicative difficulties. Instead, atypical development of action-perception circuits carrying higher cognitive processes derail aspects of language and conceptual processing which may entail further difficulties in communication, social interaction, and thought.

Further investigation is clearly necessary as to the relationship between motor system dysfunction and the development of other symptoms of ASC. One limitation of the present study is the lack of rigorous in-study diagnosis of ASC and of an overt behavioral measure of motor dysfunction. The inclusion criteria of our experiment strictly excluded those with “suspected” ASC and all individuals who had not received a previous formal diagnosis, and as such we were confident of the diagnostic status of our ASC participants. Here, the lack of motor systems response to word and action word processing was taken to reflect abnormality in these underlying systems, but future work might look in parallel at surface motor symptoms of such abnormalities, and relate them in greater detail to autistic symptoms as captured by gold-standard diagnostic instruments. Though movement abnormalities have been neglected in autism research, a causal dependence of cognitive and semantic capacities on motor systems, if demonstrated empirically, could have substantial implications for conceptualization of and interventions for ASC.

Whilst the majority of our discussion has focused on the deficit specific for action words in this population, a final note for consideration concerns the processing of visual object words. It has been suggested that individuals with ASC depend more on perceptual, perhaps more surface-level strategies of processing, rather than deep semantic analysis (Kamio and Toichi, 2000; Toichi and Kamio, 2001,2002,2003; Harris et al., 2006; Kana et al., 2006; Mottron et al., 2006; Gaffrey et al., 2007). Despite showing substantial activity in inferior temporal cortex, ASC participants did not activate this region significantly more than typically developed controls whilst reading, though the task in the present study is not directly comparable to previous findings as it involved passive reading and therefore minimal processing demands. Strength in visual or perceptual processing might, however, be supported by the relative sparing of visual object words in ASC participants, who were slower than controls at semantically judging action but not object words. In the typical population, object words also evoke activity in motor systems which relates in a somatotopic manner to the primary affordances of the concept denoted: tool words evoke activity in dorsal motor system (hand area) and the left cerebellar hemisphere which controls the right hand of the body, and food words activate dorsal portions of the motor system related to the face and mouth (Carota et al., 2012). Such motor activity, reflecting action semantic knowledge related to object affordances, appeared to be preserved here in ASC, a finding which sits parallel to the lack of a group difference in object word-induced brain activation. It appears that the direct linkage between an action word and the action it denotes is degraded in ASC, whilst the more indirect relationship between an object word and the affordances of the concept remains intact; but further investigation is required to assess this possibility and why, furthermore, object words might hold a privileged place in processing in ASC (at least compared with action words). The bias towards visual processing in ASC (Mottron et al., 2006) might provide a protective factor for words with primarily visual semantic associations. Another possibility is that action words, alongside their particular dependence on motor schemas, are additionally jeopardized by the social-pragmatic information intrinsic to their nature. Unlike object words, all action words imply an actor and several of the action words in this experiment had social associations (e.g., “speak,” “smile,” and “kiss”), and might therefore be specially problematic given the fundamental social handicap in ASC (Baron-Cohen, 2009). A third possibility is that the deficit seen here reflects a generic abnormality for processing the lexical verb class rather than an abnormality for words with action meaning per se. Strong neuropsychological and neurophysiological data suggests that the organization of meaning in the brain is driven by semantic rather than lexical differences (Vigliocco et al., 2011; Cappa and Pulvermüller, 2012; Kemmerer et al., 2012; Kiefer and Pulvermüller, 2012), but the present study cannot speak to this in ASC and so that, at present, we cannot refute with certainty the possibility that other morphosyntactic differences between nouns and verbs might result in the difference seen here between action and object words. Future research might choose to study different types of verbs (for example, abstract nouns and verbs such as “beauty” and “contemplate”) in ASC, to investigate whether the action word deficit observed in the present work relates to lexical category or to the action semantic content of these words.

In contrast to TD control subjects, ASC participants do not significantly activate cortical motor-executive systems during language processing and show corresponding difficulties processing the action-related meaning of words. Crucially, motor hypoactivation predicted, and significantly correlated with, these semantic processing difficulties, consistent with a causal role of motor-executive systems in processing action-related meaning. Motor hypoactivity also predicted the severity of autistic traits, thus suggesting a further relationship between dysfunction of motor systems and wider traits typical in ASC. More research is needed to elucidate the putative role of neural motor systems in ASC and, more generally, in social cognition and theory of mind.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.