Our findings demonstrate that this simple experimental paradigm can be used to study the online crosstalk between language and the motor systems in an ecological and economical manner. Our data further confirm that the motor brain structures that can be called upon during action word processing are not mandatorily involved; the crosstalk is asymmetrically governed by the linguistic context and not vice versa.

Participants listened to spoken action target words in either affirmative or negative sentences while holding a sensor in a precision grip. The participants were asked to count the sentences containing the name of a country to ensure attention. The grip force signal was recorded continuously. The action words elicited an automatic and significant enhancement of the grip force starting at approximately 300 ms after target word onset in affirmative sentences; however, no comparable grip force modulation was observed when these action words occurred in negative contexts.

Studies demonstrating the involvement of motor brain structures in language processing typically focus on time windows beyond the latencies of lexical-semantic access. Consequently, such studies remain inconclusive regarding whether motor brain structures are recruited directly in language processing or through post-linguistic conceptual imagery. In the present study, we introduce a grip-force sensor that allows online measurements of language-induced motor activity during sentence listening. We use this tool to investigate whether language-induced motor activity remains constant or is modulated in negative, as opposed to affirmative, linguistic contexts.

Introduction

Traditionally examined by linguists and philosophers, the mental representation of the lexical meaning is now being explored by neuroscientists and cognitive psychologists, generating a large body of sometimes conflicting experimental results and debates (see, for example, [1],[2],[3],[4],[5],[6]). In this context, studies have focused on localizing the neural correlates of word comprehension in the brain ([7],[8],[9]; for a review, see [10]). With solid evidence for the involvement of sensorimotor systems in language processing (for a review, see [11]), the systematic investigation of the interaction between neuronal language systems and sensorimotor structures should provide illuminating clues as to the role of these structures in language processing. Presently, however, the neural crosstalk between language and sensorimotor systems remains poorly understood, in part because most neuroimaging and behavioral studies do not allow the determination of whether motor involvement could be an epiphenomenal, post-comprehension process (e.g., motor intention, motor imagery, and so on) (see [12]) or whether such involvement must be understood as an intrinsic part of the lexical meaning (see [1],[13]). Furthermore, given that on the one hand, fMRI measurements of hemodynamic responses provide poor temporal resolution, and on the other hand, behavioral reaction times (RTs) are measured only after linguistic stimulus presentation, such experimental measures cannot determine whether language-induced sensorimotor activity is a cause or a consequence of lexical-semantic processing. Experimental techniques employed to avoid such temporal resolution problems, such as electroencephalography (EEG) (e.g., [14],[15],[16]) or transcranial magnetic stimulation (TMS) ([17],[18]) can be complex or remote and are not always ecologically sound. Simpler techniques that allow the capture of the online effects of language processing on sensorimotor structures would certainly advance our understanding of the role of these structures in language processing. The goal of the present study is to introduce such a tool while simultaneously assessing the role of the linguistic context on lexically induced motor activity.

At present, only a handful of studies have investigated action-word induced motor-activation in a sentential context rather than in isolation (see [19],[20],[21],[13],[15]). An investigation of the effects of the linguistic context on language-induced motor activation is critical to distinguish among the alternative accounts of observed language-induced sensorimotor activity.

The associative learning model ([22],[17]), which can be considered to be part of the group of embodied theories (see [23]), suggests that links between language and sensorimotor structures develop through simple associative learning. Inspired by the Hebbian theory of learning ([24]), this model proposes that in word learning, the simultaneous activation of language-involved areas and sensorimotor areas involved in action leads to pronounced increases in the synaptic strength between the cells of both areas, generating a functional unity. That is, assuming that “action words” (mostly verbs) are generally acquired and experienced along with the execution of the depicted actions (temporal contiguity) ([25]), this account suggests that the co-activation of the neural networks that include perisylvian language areas and motor areas emerges with experience. Through these shared circuits, the percept of an action word then automatically co-activates motor regions of the brain.

A recent study in which adult participants learned to associate novel words with novel actions confirmed that such co-activation networks can develop rapidly, within a few hours of training ([26]). Thus, this simple associative learning model predicts that brain motor activity induced by an action word should be observed whenever the action word is perceived, independent of the linguistic context in which it occurs (see [17],[27]). Note, however, that words do not consistently trigger the same motor information in all contexts. For example, Hoening and collaborators ([28]) have shown that the neural signature of a concept such as knife depends on the feature of the concept that has to be retrieved in the task (e.g., dominant attribute “to cut” vs. non-dominant attribute “elongated”) (see also [29],[30]). If the context can affect language-induced sensorimotor activity, then the simple associative learning account of the word meaning cannot hold.

In contrast with the associative learning model, theories of “Secondary Embodiment” ([12],[31]) proposes that semantic representations are amodal, such that concepts are represented independently of sensorimotor information. These latter models explain language-induced sensorimotor activity though “spreading activation” from regions that code amodal concept representations towards structures that code for sensorimotor representations once the word meaning has already been elaborated (Patterson and colleagues ([31]) suggested the anterior temporal lobe as potential location for such an amodal semantic system). Without denying the possible role of sensorimotor activity in language processing (e.g., enriching word content), a corollary of such models is that sensorimotor systems are not obligatory for the retrieval of the word meaning. Considering that no definitive answer (positive or negative) follows directly from the currently available data (for a review, see [23]), the role of sensorimotor systems in language processing remains unclear. Basic issues, such as a precise description of the crosstalk between language and motor systems, are still missing, and the conditions under which motor structures are recruited during language processing remain to be determined. Answering the question of whether language-induced motor activation is context-dependent or fixed to action concepts will help in evaluating the alternative accounts for the action-language crosstalk outlined above.

In the present study, we explored the impact of sentential negation to assess the degree of context dependency of motor activation in word processing. Sentential negation is a semantic operator that is typically encoded by a specialized morpheme that reverses the truth value of a proposition. Several cognitive aspects of negation have been explored (for a review, see [20]); however, thus far there has been little research on the effects of negation on language-induced sensorimotor activity. Certain studies have suggested that negation could reduce the access to the conceptual representation of the negated items ([32],[33]). For instance, MacDonald and Just ([32]), who compared the speed of word retrieval in affirmative and negative contexts found that negated words (e.g., “no cookies”) yielded significantly longer response times. The mechanism underlying this behavioral phenomenon, however, remains unclear. Certain authors (cf. [34], [35]) assume that understanding a negated sentence (e.g., “The door is not open”) requires building an initial representation of the corresponding positive state of affair (e.g., “The door is open”), which is then rejected. According to this view, if the representation of an action word involves neural motor structures, the negated actions should first activate and then inhibit the corresponding motor regions. Currently available neuroimaging ([36],[21]) and TMS data ([37]) on the sentential negation of action terms have shown that negated actions display weaker activation in the cortical motor structures than comparable affirmative ones. Because of technical constraints, however, none of these previous studies allowed the fine-grained temporal analysis that would be required to determine whether reduced motor activity occurs after an initial phase of motor activation or whether negation simply leaves the motor structures less active. Note that although an activation-inhibition picture is compatible with a purely associative learning model, inactivation is not.

The goals of the present study were as follows: (1) to introduce a novel experimental tool, a grip-force sensor (ATI mini-40) that provides the means to make online and direct measurements of the effects of language processing on motor activity ([38]) and (2) to investigate the time course of language-induced motor activation and its sensitivity to the linguistic context by presenting hand-related action words in positive or negative sentences while monitoring how the motor activation component is affected by this syntactic construction. Participants were asked to listen to spoken sentences that contained the action target words embedded within affirmative or negative contexts. Throughout the experiment, the participants held the sensor in a precision grip with their right hand (the thumb, index and middle fingers were in contact with the load cell) such that the grip force signal was registered continuously across a given time interval. A previous study by Frak et al. ([38]) established that this type of sensor can capture subtle grip force variations while subjects listen to single words. In that study, participants listened to words relating (verbs) or not relating (nouns) to a manual action while holding a cylinder with an integrated force sensor. The authors found a change in the grip force when the subjects heard verbs that related to manual action. The grip force increased from approximately 100 ms following the verb presentation and peaked at 380 ms. These observations reveal the relationship that exists between language and grasp and show that it is possible to elucidate new aspects of sensorimotor interaction online.

To attenuate the possibility of mental-imagery effects on motor activation, we avoided the first-person perspective in our sentences and used the third-person perspective instead. It has been shown that first-person process involves mostly a kinesthetic representation of the action, whereas the third-person perspective is much more conducive to visual imagery (see [39],[40]). Moreover, no motor task associated with the linguistic process was required, as the participants were asked to count how many sentences contained the name of a country. This task ensured that potential grip force effects were elicited only by listening to action sentences.

To interpret the time course of language-induced motor activation, we drew on an influential neurophysiological model of spoken sentence comprehension, temporal parameters of which were based on electrophysiological data ([41]). According to this model, information about syntactic structure is formed based on information about word category approximately 100–300 ms after word onset in a first phase. In a second phase (300–500 ms), lexical-semantic and morphosyntactic processes are computed for thematic role assignment. In a third and final phase (500–1000 ms), the information generated in phases 1 and 2 is integrated and reanalyzed. Despite the definition into three discrete time windows, we assume that the processes identified in the model could occur gradually. While observation of language-induced grip force modulation within these different time windows does not automatically imply a causal link between the motor and the language processes, referring to this model will nonetheless allow formulating some clear predictions. Hence, if the motor representation of the action is part of the lexical-semantic representation of the action words, we should expect the following: