Contribution of the primary motor cortex to motor imagery: a subthreshold TMS study

Motor imagery (MI) mostly activates the same brain regions as movement execution (ME) including the primary motor cortex (Brodmann area 4, BA4). However, whether BA4 is functionally relevant for MI remains controversial. The finding that MI tasks are impaired by BA4 virtual lesions induced by transcranial magnetic stimulation (TMS) supports this view, though previous studies do not permit to exclude that BA4 is also involved in other processes such as hand recognition. Additionally, previous works largely underestimated the possible negative consequences of TMS-induced muscle twitches on MI task performance. Here we investigated the role of BA4 in MI by interfering with the function of the left or right BA4 in healthy subjects performing a MI task in which they had to make laterality judgements on rotated hand drawings. We used a subthreshold repetitive TMS protocol and monitored electromyographic activity to exclude undesirable effects of hand muscle twitches. We found that BA4 virtual lesions selectively increased reaction times in laterality judgments on hand drawings, leaving unaffected a task of equal difficulty, involving judgments on letters. Interestingly, the effects of virtual lesions of left and right BA4 on MI task performance were the same irrespective of the laterality (left/right) of hand drawings. A second experiment allowed us to rule out the possibility that BA4 lesions affect visual or semantic processing of hand drawings. Altogether, these results indicate that BA4 contribution to MI tasks is specifically related to the mental simulation process and further emphasize the functional coupling between ME and MI.     

The role of the premotor cortex and the primary motor cortex in action verb comprehension: evidence from Granger causality analysis

Although numerous studies find the premotor cortex and the primary motor cortex are involved in action language comprehension, so far the nature of these motor effects is still in controversy. Some researchers suggest that the motor effects reflect that the premotor cortex and the primary motor cortex make functional contributions to the semantic access of action verbs, while other authors argue that the motor effects are caused by comprehension. In the current study, we used Granger causality analysis to investigate the roles of the premotor cortex and the primary motor cortex in processing of manual-action verbs. Regions of interest were selected in the primary motor cortex (M1) and the premotor cortex based on a hand motion task, and in the left posterior middle temporal gyrus (lexical semantic area) based on the reading task effect. We found that (1) the left posterior middle temporal gyrus had a causal influence on the left M1; and (2) the left posterior middle temporal gyrus and the left premotor cortex had bidirectional causal relations. These results suggest that the premotor cortex and the primary motor cortex play different roles in manual verb comprehension. The premotor cortex may be involved in motor simulation that contributes to action language processing, while the primary motor cortex may be engaged in a processing stage influenced by the meaning access of manual-action verbs. Further investigation combining effective connectivity analysis and technique with high temporal resolution is necessary for better clarification of the roles of the premotor cortex and the primary motor cortex in action language comprehension.     

Cognitive motor processes: The role of motor imagery in the study of motor representations

Motor imagery is viewed as a window to cognitive motor processes and particularly to motor control. Mental simulation theory [Jeannerod, M., 2001. Neural simulation of action: a unifying mechanism for motor cognition. NeuroImage 14, 103–109] stresses that cognitive motor processes such as motor imagery and action observation share the same representations as motor execution. This article presents an overview of motor imagery studies in cognitive psychology and neuroscience that support and extend predictions from mental simulation theory. In general, behavioral data as well as fMRI and TMS data demonstrate that motor areas in the brain play an important role in motor imagery. After discussing results on a close overlap between mental and actual performance durations, the review focuses specifically on studies reporting an activation of primary motor cortex during motor imagery. This focus is extended to studies on motor imagery in patients. Motor imagery is also analyzed in more applied fields such as mental training procedures in patients and athletes. These findings support the notion that mental training procedures can be applied as a therapeutic tool in rehabilitation and in applications for power training.     

Knowing the Meaning of a Word by the Linguistic and Perceptual Company It Keeps

Debates on meaning and cognition suggest that an embodied cognition account is exclusive of a symbolic cognition account. Decades of research in the cognitive sciences have, however, shown that these accounts are not at all mutually exclusive. Acknowledging cognition is both symbolic and embodied generates more relevant questions that propel, rather than divide, the cognitive sciences: questions such as how computational symbolic findings map onto experimental embodied findings, and under what conditions cognition is relatively more symbolic or embodied in nature. The current paper revisits the Symbol Interdependency Hypothesis, which argues that language encodes perceptual information and that language users rely on these language statistics in cognitive processes. It argues that the claim that words are abstract, amodal, and arbitrary symbols and therefore must always be grounded to become meaningful is an oversimplification of the language system. Instead, language has evolved such that it maps onto the perceptual system, whereby language users rely on language statistics, which allow for bootstrapping meaning also when grounding is limited.     

Language is a Source of Grounding and a Mode of Action

Kemmerer argues that grounded cognition explains how language-specific semantic structures can influence nonlinguistic cognition. In this commentary, I argue that his proposal fails to fully consider the possibility that language itself can serve as a source of grounding. Our concepts are not merely shaped by a disembodied language system; they emerge in the context of linguistic experience and action. This inclusive approach to grounded cognition offers an expanded conception of the phenomena associated with linguistic relativity. I provide empirical and theoretical reasons to adopt this theoretical perspective.     

Supplementary motor area and primary auditory cortex activation in an expert break-dancer during the kinesthetic motor imagery of dance to music

The current study used functional magnetic resonance imaging to examine the neural activity of an expert dancer with 35 years of break-dancing experience during the kinesthetic motor imagery (KMI) of dance accompanied by highly familiar and unfamiliar music. The goal of this study was to examine the effect of musical familiarity on neural activity underlying KMI within a highly experienced dancer. In order to investigate this in both primary sensory and motor planning cortical areas, we examined the effects of music familiarity on the primary auditory cortex [Heschl’s gyrus (HG)] and the supplementary motor area (SMA). Our findings reveal reduced HG activity and greater SMA activity during imagined dance to familiar music compared to unfamiliar music. We propose that one’s internal representations of dance moves are influenced by auditory stimuli and may be specific to a dance style and the music accompanying it.     

Focal enhancement of motor cortex excitability during motor imagery: a transcranial magnetic stimulation study

OBJECTIVES: In order to learn more about the physiology of the motor cortex during motor imagery, we evaluated the changes in excitability of two different hand muscle representations in the primary motor cortex (M1) of both hemispheres during two imagery conditions. MATERIALS AND METHODS: We applied focal transcranial magnetic stimulation (TMS) over each M1, recording motor evoked potentials (MEPs) from the contralateral abductor pollicis brevis (APB) and first dorsal interosseus (FDI) muscles during rest, imagery of contralateral thumb abduction (C-APB), and imagery of ipsilateral thumb abduction (I-APB). We obtained measures of motor threshold (MT), MEP recruitment curve (MEP-rc) and F waves. RESULTS: Motor imagery compared with rest significantly decreased the MT and increased MEPs amplitude at stimulation intensities clearly above MT in condition C-APB, but not in condition I-APB. These effects were not significantly different between right and left hemisphere. MEPs simultaneously recorded from the FDI, which was not involved in the task, did not show facilitatory effects. There were no significant changes in F wave amplitude during motor imagery compared with rest. CONCLUSIONS: Imagery of unilateral simple movements is associated with increased excitability only of a highly specific representation in the contralateral M1 and does not differ between hemispheres.     

Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study

OBJECTIVE: Cerebral [18F]fluorodeoxy-D-glucose PET ([18F]FDG-PET) was used to visualize the lasting neuronal activation after repetitive transcranial magnetic stimulation (rTMS) over the left hand area of the primary motor cortex (M1HAND). BACKGROUND: Applied over M1HAND, rTMS has been shown to produce a modulation of corticomotor excitability beyond the time of stimulation itself. METHODS: Eight right-handed subjects underwent nonquantitative [18F]FDG-PET measurements during two experimental conditions: at rest and after focal subthreshold 5-Hz rTMS over the left M1HAND. In the post-rTMS condition, [18F]FDG was injected immediately after the administration of 1,800 magnetic pulses over the left M1HAND. Relative differences in normalized regional cerebral metabolic rate of glucose (normalized rCMRglc) between conditions were determined using a voxel-by-voxel Student's t-test and volume-of-interest (VOI) analysis. Analysis was a priori restricted to the M1HAND, the supplementary motor area (SMA), and the primary auditory cortex of both hemispheres. RESULTS: A 5-Hz rTMS of the left M1HAND caused a lasting relative increase in normalized rCMRglc within the M1HAND bilaterally and the SMA. The magnitude and the topographic pattern of persisting relative rCMRglc increases within these motor cortical areas demonstrated considerable interindividual variations. CONCLUSIONS: Subthreshold 5-Hz repetitive transcranial magnetic stimulation (rTMS) over the hand area of the primary motor cortex is associated with a persisting neuronal activation in a distinct set of motor cortical areas beyond the time of stimulation. The current findings demonstrate that [18F]FDG-PET can localize and quantify regional net changes in synaptic cortical activity after rTMS and thus might elucidate the mechanisms underlying rTMS-associated therapeutic effects.     

The representation of the plegic hand in the motor cortex: a combined fMRI and TMS study

TMS mapping and fMRI were used to investigate changes in the motor cortex representation of the hand in a patient with complete loss of right hand function following traumatic avulsion of the cervical roots C7 and C8. Both TMS and fMRI demonstrated an expansion of the motor representation of the forearm into the hand area contralateral to the injured side. fMRI of the hand area, however, revealed that this area could still be activated when the patient was instructed to imagine finger tapping with his plegic hand. These results indicate that the plegic hand is still represented in the motor cortex, despite the fact that the same cortical area is also now active during movements involving forearm muscles.     

Motor imagery: a window into the mechanisms and alterations of the motor system

Motor imagery is a widely used paradigm for the study of cognitive aspects of action control, both in the healthy and the pathological brain. In this paper we review how motor imagery research has advanced our knowledge of behavioral and neural aspects of action control, both in healthy subjects and clinical populations. Furthermore, we will illustrate how motor imagery can provide new insights in a poorly understood psychopathological condition: conversion paralysis (CP). We measured behavioral and cerebral responses with functional magnetic resonance imaging (fMRI) in seven CP patients with a lateralized paresis of the arm as they imagined moving the affected or the unaffected hand. Imagined actions were either implicitly induced by the task requirements, or explicitly instructed through verbal instructions. We previously showed that implicitly induced motor imagery of the affected limb leads to larger ventromedial prefrontal responses compared to motor imagery of the unaffected limb. We interpreted this effect in terms of greater self-monitoring of actions during motor imagery of the affected limb. Here, we report new data in support of this interpretation: inducing self-monitoring of actions of both the affected and the unaffected limb (by means of explicitly cued motor imagery) abolishes the activation difference between the affected and the unaffected hand in the ventromedial prefrontal cortex. Our results show that although implicit and explicit motor imagery both entail motor simulations, they differ in terms of the amount of action monitoring they induce. The increased self-monitoring evoked by explicit motor imagery can have profound cerebral consequences in a psychopathological condition.     

Contribution from neurophysiological and psychological methods to the study of motor imagery

This paper reviews studies on neurophysiological and behavioral methods used to evaluate motor imagery accuracy. These methods can be used when performed in the field and are based on recordings of peripheral indices such as autonomic nervous system or electromyographic activities, mental chronometry and psychological tests. Providing physiological signs that correlate to these types of mental processes may be considered an objective approach for motor imagery analysis. However, although autonomic nervous system activity recording has been shown to match motor imagery in real time, to evaluate its accuracy qualitatively and the individual ability to form mental images, the relationship between physiological responses and mental processes remains an inference. Moreover, electromyographic recordings may be associated with postural control data, but due to inconsistent results, they remain insufficient to solely evaluate motor imagery accuracy. Other techniques traditionally used in psychology and cognitive psychology are questionnaires, “debriefing” with subjects and mental chronometry. Although such methods lead to interesting results, there remains an important part of subjectivity as subjects perform an autoevaluation of motor imagery accuracy. Similarly, mental chronometry gives information on the ability to preserve temporal organization of movement but does not allow the evaluation of the vividness of mental images. Thus, several methods should be combined to analyze motor imagery accuracy in greater detail. Neurophysiological recordings cannot therefore be considered an alternative but rather a complementary technique to behavioral and psychological methods. The advantages and inconvenient of each technique and the hypotheses that could be tested are discussed.     

Attention, motor control and motor imagery in schizophrenia: implications for the role of the parietal cortex

Many recent models of schizophrenia have attempted to explain the so-called first-rank symptoms in terms of a breakdown in the self-monitoring of thoughts and behaviours. These models have focused on the most common symptom of schizophrenia auditory hallucinations—suggesting that they may represent disordered self-monitoring of internal speech. As such, much attention has been given to the role of the temporal and frontal cortices in the clinical presentation of patients with schizophrenia. In this review, we examine the role of the posterior parietal cortex (PPC) in schizophrenia within the context of recent models of self-monitoring deficits in these patients. Attentional dysfunctions and certain impairments of motor control and motor imagery all point towards the involvement of the parietal cortex in the disorder. In particular, we suggest that patients experiencing passivity phenomena (e.g., delusions of control) may have particular impairments of parietal function related to poor utilisation of forward models of intended actions. We also present a novel hypothesis that suggests differential impairments of the left and right parietal cortices in schizophrenia may help explain many of the first-rank symptoms of the disorder.     

Motor cortex hand area and speech: implications for the development of language

Recently a growing body of evidence has suggested that a functional link exists between the hand motor area of the language dominant hemisphere and the regions subserving language processing. We examined the excitability of the hand motor area and the leg motor area during reading aloud and during non-verbal oral movements using transcranial magnetic stimulation (TMS). During reading aloud, but not before or afterwards, excitability was increased in the hand motor area of the dominant hemisphere. This reading effect was found to be independent of the duration of speech. No such effect could be found in the contralateral hemisphere. The excitability of the leg area of the motor cortex remained unchanged during reading aloud. The excitability during non-verbal oral movements was slightly increased in both hemispheres. Our results are consistent with previous findings and may indicate a specific functional connection between the hand motor area and the cortical language network.     

Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers

This paper describes the quantitative areal and laminar distribution of identified neuron populations projecting from areas of prefrontal cortex (PFC) to subcortical autonomic, motor, and limbic sites in the rat. Injections of the retrograde pathway tracer wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP) were made into dorsal/ventral striatum (DS/VS), basolateral amygdala (BLA), mediodorsal thalamus (MD), lateral hypothalamus (LH), mediolateral septum, dorsolateral periaqueductal gray, dorsal raphe, ventral tegmental area, parabrachial nucleus, nucleus tractus solitarius, rostral/caudal ventrolateral medulla, or thoracic spinal cord (SC). High-resolution flat-map density distributions of retrogradely labelled neurons indicated that specific PFC regions were differentially involved in the projections studied, with medial (m)PFC divided into dorsal and ventral sectors. The percentages that WGA-HRP retrogradely labelled neurons composed of the projection neurons in individual layers of infralimbic (IL; area 25) prelimbic (PL; area 32), and dorsal anterior cingulate (ACd; area 24b) cortices were calculated. Among layer 5 pyramidal cells, approximately 27.4% in IL/PL/ACd cortices projected to LH, 22.9% in IL/ventral PL to VS, 18.3% in ACd/dorsal PL to DS, and 8.1% in areas IL/PL to BLA; and 37% of layer 6 pyramidal cells in IL/PL/ACd projected to MD. Data for other projection pathways are given. Multiple dual retrograde fluorescent tracing studies indicated that moderate populations (<9%) of layer 5 mPFC neurons projected to LH/VS, LH/SC, or VS/BLA. The data provide new quantitative information concerning the density and distribution of neurons involved in identified projection pathways from defined areas of the rat PFC to specific subcortical targets involved in dynamic goal-directed behavior.     

Role of the primary motor and sensory cortex in precision grasping: a transcranial magnetic stimulation study

Human precision grip requires precise scaling of the grip force to match the weight and frictional conditions of the object. The ability to produce an accurately scaled grip force prior to lifting an object is thought to be the result of an internal feedforward model. However, relatively little is known about the roles of various brain regions in the control of such precision grip-lift synergies. Here we investigate the role of the primary motor (M1) and sensory (S1) cortices during a grip-lift task using inhibitory transcranial magnetic theta-burst stimulation (TBS). Fifteen healthy individuals received 40 s of either (i) M1 TBS, (ii) S1 TBS or (iii) sham stimulation. Following a 5-min rest, subjects lifted a manipulandum five times using a precision grip or completed a simple reaction time task. Following S1 stimulation, the duration of the pre-load phase was significantly longer than following sham stimulation. Following M1 stimulation, the temporal relationship between changes in grip and load force was altered, with changes in grip force coming to lag behind changes in load force. This result contrasts with that seen in the sham condition where changes in grip force preceded changes in load force. No significant difference was observed in the simple reaction task following either M1 or S1 stimulation. These results further quantify the contribution of the M1 to anticipatory grip-force scaling. In addition, they provide the first evidence for the contribution of S1 to object manipulation, suggesting that sensory information is not necessary for optimal functioning of anticipatory control.     

Value judgments and self-control of action: The role of the medial frontal cortex

Humans generate actions in relation to perceived events in the environment. Events are valuated in terms of subjective (personal) relevance or meaning, i.e. “what does this mean to me?”. Similarly, making sense or gaining meaning from sensations (i.e., “perception”) from one's own body and of mental images, such as memories or intentions, involves valuation from a subjective perspective. Here, we review recent findings in neurophysiology and neuroimaging suggesting that the medial frontal cortex comprises cortical relay nodes that afford the attribution of self-relevant, immediate and intuitive (implicit) meaning. In addition, we describe recent data that suggest that the medial frontal cortex participates also in the explicit appraisal of certain stimuli, namely, emotional face expressions, occurring as early as 150 ms following the stimulus. We propose that the medial frontal cortex subserves egocentric “value” judgments (both implicit and explicit), which are critical for self-control of action.     

The influence of rTMS over prefrontal and motor areas in a morphological task: grammatical vs. semantic effects

We investigated the differential role of two frontal regions in the processing of grammatical and semantic knowledge. Given the documented specificity of the prefrontal cortex for the grammatical class of verbs, and of the primary motor cortex for the semantic class of action words, we sought to investigate whether the prefrontal cortex is also sensitive to semantic effects, and whether the motor cortex is also sensitive to grammatical class effects. We used repetitive transcranial magnetic stimulation (rTMS) to suppress the excitability of a portion of left prefontal cortex (first experiment) and of the motor area (second experiment). In the first experiment we found that rTMS applied to the left prefrontal cortex delays the processing of action verbs' retrieval, but is not critical for retrieval of state verbs and state nouns. In the second experiment we found that rTMS applied to the left motor cortex delays the processing of action words, both name and verbs, while it is not critical for the processing of state words. These results support the notion that left prefrontal and motor cortex are involved in the process of action word retrieval. Left prefrontal cortex subserves processing of both grammatical and semantic information, whereas motor cortex contributes to the processing of semantic representation of action words without any involvement in the representation of grammatical categories.     

Segregating two inhibitory circuits in human motor cortex at the level of GABAA receptor subtypes: a TMS study.

OBJECTIVE: To investigate if different interneuronal circuits in human motor cortex mediate inhibition through different subtypes of the gamma-aminobutyric acid A receptor (GABAAR). METHODS: Two distinct forms of motor cortical inhibition were measured in 10 healthy subjects by established transcranial magnetic stimulation (TMS) protocols: short interval intracortical inhibition (SICI) and short latency afferent inhibition (SAI). Their modification by a single oral dose of three different positive GABAAR modulators (20 mg of diazepam, 2.5 mg of lorazepam and 10 mg of zolpidem) with different affinity profiles at the various alpha-subunit bearing subtypes of the GABAAR (diazepam: non-selective, lorazepam: unknown, zolpidem: 10-fold higher affinity to alpha1- than alpha2- or alpha3-subunit bearing GABAARs, no affinity to alpha5-subunits) was tested in a randomized crossover design. In addition, the sedative drug effects were recorded by a visual analogue scale. RESULTS: Diazepam and lorazepam increased SICI, whereas zolpidem did not change SICI. In contrast, diazepam had no effect on SAI, whereas lorazepam and zolpidem decreased SAI. The sedative effects were not different between drugs. CONCLUSIONS: The dissociating patterns of drug modification of SICI versus SAI strongly suggest that different GABAAR subtypes are involved in SICI and SAI. SIGNIFICANCE: We provide evidence, for the first time, for a dissociation of effects of diazepam and zolpidem on SAI and confirm the previously reported differential effect of zolpidem and of diazepam and lorazepam on SICI. The differential effects of the three benzodiazepines on SAI and SICI suggest that neuronal circuits in human motor cortex that mediate inhibition through different GABAAR subtypes can be segregated by TMS.     

Hand motor cortex activation in a patient with congenital mirror movements: a study of the silent period following focal transcranial magnetic stimulation

Motor evoked potentials (MEPs) to focal transcranial magnetic stimulation (TMS) have demonstrated that abnormal ipsilateral corticospinal projections are active in patients with congenital mirror movements. In addition, movement-related potentials and PET suggest that an abnormal pattern of motor cortex activation could be associated with an anomaly of the corticospinal tracts. In the present study the silent period (SP) following focal TMS was investigated in a woman with familial congenital mirror movements. Recordings were made from both the abductor pollicis brevis (APB) muscles. When focal TMS was delivered during an intended contralateral APB muscle contraction, MEP and SP were bilaterally recorded and SP was significantly shorter than the contralateral SP observed in normal controls. An abnormal bilateral activation of the hand motor cortex can explain our findings. The non-stimulated motor cortex causes an early partial recovery of the background EMG activity when the stimulated motor cortex is still inhibited (beginning as soon as the transcallosal and the short-lasting segmental inhibition are both complete.