Explaining the muscular activity observed during inner speech

Motor imagery can be defined as the mental process by which one rehearses a given action, without engaging in the physical movements involved in this particular action. One of the most influential theoretical explanation for this phenomenon is themotor simulation theory (MST, Jeannerod, 1994, 2001, 2006). In this framework, the concept of simulation refers to the

“offline rehearsal of neural networks” (Jeannerod, 2006) and motor imagery is conceptualised as a simulation of the covert (i.e., invisible and inaudible to an external observer) stage of the same executed action (O’Shea & Moran, 2017). The MST shares some similarities with the theories of embodied and grounded cognition (Barsalou, 2008) in that both allow to account for motor imagery by appealing to a simulation mechanism. However, the concept of simulation in grounded theories is assumed to be multi-modal (not just motoric) and to operate in order to acquire specific conceptual knowledge (O’Shea & Moran, 2017), which is not the concern of the MST.¹⁶ As highlighted by O’Shea & Moran (2017), the MST contains

15While keeping in mind the obvious limitation that the child mind is not equivalent to the adult mind, nor is it equivalent to a smaller version of the adult mind. Nevertheless, examining the development of novel imagined actions in adults avoids the contamination of the process of interest (imagined action) by developmental confounds present during childhood.

16We should also make a distinction betweenembodiment of content, which concerns the semantic content of language, andembodiment of form, which concerns “the vehicle of thought”, that is, proper verbal production

the three following postulates at its core: i) there exists a continuum between the covert (the mental representation) and the overt execution of an action, ii) action representations can operate off-line, via a simulation mechanism, and iii) covert actions rely on the same set of mechanisms as the overt actions they simulate, except that execution is inhibited. The MST is supported by a wealth a findings, going from mental chronometry studies showing that the time taken to perform an action is often found to be similar to the time needed to imagine the corresponding action¹⁷(but see Glover & Baran, 2017, for a review of chronometric findings and for an alternative conceptualisation of motor imagery), to neuroimaging and neurostimulation studies showing that both motor imagery and overt actions tend to recruit similar frontal, parietal and sub-cortical regions (e.g., Hétu et al., 2013; Jeannerod, 2001).

The involvement of the motor system during motor imagery is also supported by repeated observations of autonomic responses, increased corticospinal excitability, as well as peripheral muscular activity during motor imagery (for an overview, see Collet & Guillot, 2010; Jeannerod, 2006; Stinear, 2010).

Motor imagery has consistently been defined as the mental rehearsal of a motor action without any overt movement. One consequence of this claim is that, in order to prevent execution, the neural commands for muscular contractions should be blocked at some level of the motor system by active inhibitory mechanisms (for review, see Guillot et al., 2012a).

Despite these inhibitory mechanisms, there is now abundant evidence for peripheral muscular activation during motor imagery (for review, see Guillot & Collet, 2005; Guillot et al., 2012a).

As suggested by Jeannerod (1994), the incomplete inhibition of the motor commands would provide a valid explanation to account for the peripheral muscular activity observed during motor imagery. Consistent with this assumption, Schwoebel, Boronat, & Branch Coslett (2002) showed that a brain-damaged patient failed to inhibit the motor consequences of motor imagery, and thus fully “executed the imagined action”, hence highlighting uninhibited movements during mental rehearsal.¹⁸ This idea has also been corroborated by studies of changes in the excitability of the motor pathways during motor imagery tasks. Bonnet, Decety, Jeannerod, & Requin (1997) measured spinal reflexes while participants were instructed to either press a pedal with the foot or to simulate the same action mentally. They observed that both H-reflexes and T-reflexes increased during motor imagery, and that these increases correlated with the force of the simulated pressure. Using transcranial magnetic stimulation and motor evoked potentials (MEPs), several investigators observed muscle-specific increases of MEPs during various motor imagery tasks, whereas no such increase could be observed in antagonist muscles (e.g., Fadiga et al., 1999; Rossini, 1999).

(Pickering & Garrod, 2013).

17Although not always. As previously discussed in section 1.2.1, Guillot et al. (2012b) reviewed chronometric findings related to motor imagery and listed the several factors that may affect the temporal equivalence between executed and imagined actions.

18However, it should be noted that Schwoebel et al. (2002) reported no difficulty for this patient to read silently.

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Box 1.4: The motor inhibition problem

The ”problem of inhibition” can be summarised as follows (from Jeannerod, 2001, p.

S106): how come that covert actions, in spite of activation of the motor system, do not result in muscular activity and overt movements?

An attractive answer to that question is that imagined actions can be considered as inhibited actions. The neural generators of these inhibitory signals, however, have not yet been clearly identified in the motor imagery literature. As reviewed in Guillot et al. (2012a), previous research has suggested at least three (non-exclusive) potential inhibitory mechanisms that might operate during motor imagery:

• First, motor inhibition might beintegratedwithin the construction of the mental representation (i.e., imagination would simply be a weaker form of execution), hence only subthreshold (i.e., insufficient to induce motoneurons excitation) motor commands are sent to the effectors to prevent movement execution.

• Second, inhibitory mechanisms may be triggered in conjunction with motor commands (e.g., Jeannerod, 2006): inhibitory cerebral regions might progressively weaken the motor commands during the time course of motor imagery, so that only aresidualactivity is sent.

• Third, inhibitory mechanisms might be located downstream of the motor cortex, possibly at the spinal or brainsteam level (e.g., Jeannerod, 2001; 2006). Lotze &

Halsband (2006) also suggested that the posterior cerebellum might play a crucial role in inhibiting the motor commands.

Therefore, motor commands inhibition might intervene in three non-exclusive ways during motor imagery. However, the exact contribution of each route still needs to be examined.

However, although there are many observations showing a peripheral muscular activity during motor imagery, there are also many studies failing to do so, or reporting surprisingly high levels of inter-subject variability, with some participants showing no muscular activity at all (for review, see Guillot, Lebon, & Collet, 2010). Two main explanations have been advanced to resolve these discrepancies. First, the electromyographic activity recorded during motor imagery could be moderated by the perspective taken in motor imagery.¹⁹ Indeed, it has been shown that a first-person perspective may result in greater EMG activity than motor imagery in a third-person perspective (Hale, 1982; Harris & Robinson, 1986). Second, some

19We usually make a distinction between a first-person perspective orinternal imagery(i.e., imagining an action as we would execute it) and a third-person perspective orexternal imagery(i.e., imagining an action as an observer of this action), that seem to involve different neural and cognitive processes (Ruby & Decety, 2001).

authors postulated that the intensity of the EMG activity recorded during motor imagery might be related to the individual ability to form an accurate mental representation of the motor skill (i.e., the vividness of the mental image). However, after reviewing the available evidence, Guillot et al. (2009) concluded that this is unlikely to be the case. Alternatively, discrepancies in experimental design and methodological choices (e.g., use of intramuscular versus surface electromyography) could also explain these contradictory results (Guillot et al., 2010).

In order to investigate the inhibitory mechanisms involved during motor imagery, Rieger, Dahm, & Koch (2017) extended the logic of task switching paradigms and developed a novel action mode(imagery vs. execution) switching paradigm. In these procedures, performance in the current trial is analysed depending on the condition of the previous trial, assuming that execution or inhibition in the previous trial persists to a certain degree. Put simply, the main idea is that inhibition during motor imagery should leave after-effects by increasing activation thresholds, then affecting the performance of subsequently executed (or imagined) movements. In analysing sequential effects, Rieger et al. (2017) observed shorter movement times when motor execution (ME) preceded motor imagery (MI) than when motor imagery preceded motor execution, corroborating the idea of a global inhibition (i.e., the second option from Box 1.4) mechanism taking place during motor imagery. In addition, they observed hand repetition costs (i.e., movement times were longer when the task had to be performed with the same hand than with the other hand in motor imagery trials), suggesting that effector-specific inhibitory mechanisms may also taking place during motor imagery (corroborating the third option discussed in Box 1.4). However, as highlighted by O’Shea & Moran (2018), global inhibitory mechanisms may also induce longer movements times in MI-ME sequences than in ME-ME sequences, but this effect was not observed in Rieger et al. (2017). To push forward this investigation, O’Shea & Moran (2018) used pupillometry to examine the degree of attentional effort involved in the execution or the inhibition of a motor response during both motor imagery and motor execution in a Go/NoGo procedure, embedded in a modified task-switching paradigm. They observed that the amount of attentional effort (assessed via pupillometry) varied according to the type of block (i.e., pure vs. mixed), suggesting that different inhibitory mechanisms (or “routes”) may underlie inhibition during motor imagery.

For instance, it may be that inhibition during motor imagery is programmed in a pre-emptive way when the participants know that the next block will be uniquely composed of motor imagery trials or in a more active (and more effort-costly) way in mixed blocks. Therefore, different inhibitory mechanisms (e.g., proactive vs. reactive, global vs. selective) may also vary according to the task characteristics (for a more detailed discussion of these findings, see also O’Shea, 2017). Although these studies are among the first to investigate these issues, they show that it is possible to use a combination of cognitive and psychophysiological tasks to assess the inhibitory mechanisms involved during motor imagery.

To summarise this section, the available neural and psychophysiological evidence suggests that inner speech and imagined actions may result from internal simulation (or emulation)

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of the corresponding executed action. This appealing idea however presupposes that the motor commands emitted during inner speech (which give rise to the sensory percepts of inner speech such as the inner voice) are somehow completely or partially inhibited in order to prevent execution. We discussed several explanations with regards to the source of these inhibitory signals (that remains to be tested in the case of inner speech). Interestingly, these questions echo our previous discussion of the centralism versus peripheralism debate (cf. Box 1.1). Recent theoretical frameworks of inner speech and motor imagery (e.g., motor control models, simulation and emulation theories) arecentralisttheories of motor cognition.

Indeed, in these frameworks, the peripheral muscular activity observed during imagined action is conceived as a consequence of (a partial inhibition) these actions, rather than a necessarycondition for imagining actions (including speech). This idea was well summarised by Jeannerod (2006), discussing the motor inhibition problem and the case of subvocal (inner) speech:

“Subvocal speech was first interpreted as a source of peripheral kinesthetic information which, when projected to central nervous structures, generated auditory images of the corresponding words. The same interpretation was given to the low intensity EMG recorded during mental motor imagery of limb actions, which was thought to be the origin of the feelings experienced by the subject during mental rehearsal (Jacobson, 1930), or to the eye movements recorded during mental visual imagery (e.g., Brandt and Stark, 1997). However, this interpretation of mental processes as consequences of peripheral feedback is now disproved by recent experiments showing complete absence of muscular activity in many subjects during motor imagery. When present, this activity is rather assumed to be a consequence of incomplete inhibition of motor output during mental states involving motor simulation. This same interpretation might also hold for inner speech.” (p. 153)

Therefore, although the precise neural generators of these inhibitory signals remain to be examined, the peripheral muscular activation observed during inner speech may be resulting from an incomplete inhibition of motor commands. Moreover, we may speculate that some forms of inner speech may or may not be accompanied by peripheral muscular activations in the speech muscles, depending on the degree (the amount) of inhibition.