MOTOR INHIBITION DURING MOTOR IMAGERY

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MOTOR IMAGERY

DEFINITION

Motor Imagery (MI) is the mental representation of an action without concomitant body movements (Jeannerod, 1994). Similarities between MI and PP are reported from behavioral (e.g., temporal congruence Decety et al., 1989, Guillot et al., 2005a, Gueugneau et al., 2008, Papaxanthis et al., 2012, Di Rienzo et al., 2014b, Fusco et al., 2014) to neurophysiological (Hanakawa et al., 2008, Munzert et al., 2009, Guillot et al., 2014, Case et al., 2015) parameters.
Classically, while MI is by default a multimodal process, different MI modalities are considered according to the type of sensory information processed during the mental representation of the action. The most frequent MI modalities encountered in scientific protocols are i) internal and external visual MI, and ii) kinesthetic MI.
Internal visual imagery is a form of MI where the person visualizes herself performing the action from a first-person perspective (Figure 3 left), while during external visual imagery, the persons sees herself performing an action from a third-person perspective (Figure 3 right). Kinesthetic is a form of MI emphasizing the feel of the movement, force, effort, and spatial sensations, where the action is mentally represented from proprioceptive information. Overall, MI consists in the voluntary recall of procedural motor memories.
Figure 3. Motor imagery visual perspectives. Left image represent a first-person perspective of a free-throw in basketball, the imager mentally rehearses the visual information encountered by his/her eyes during the task. The right image represent a third-person perspective of the same task, imager creating images a camera would capture from a given distance.
Looking for the specificity of MI modalities, White and Hardy (1995) reported that internal MI would be more effective than external MI in goal-oriented motor tasks relying on perception (e.g., a downhill slalom). Conversely, external imagery would be better for form-based tasks, since it extracts higher order aspects of a skill (Whiting and Den Brinker, 1982, Morrison, 1991). Accordingly, Hardy and Callow (1999) examined different types of MI training designed to learn distinct motor skills, i.e., a karate kata, a gymnastic routine, and a rock climbing task. They confirmed their initial proposal (White and Hardy, 1995), that external MI might be predominantly effective when rehearsing form-based tasks (see also, Guillot et al., 2012b).

NEUROFUNCTIONAL BASES

Defining MI as a purely mental processes would imply that it is intrinsically distinct from the physical performance. However, MI represents an emulation of an internal state of action preparation (Jeannerod, 1994). There is now compelling evidence that during MI, motor command signals are processed and inhibited at some stage of the motor system (for a review, see Guillot et al., 2012a). According to Jeannerod (2001), MI shares common neural substrates with both action preparation and execution, as attested by the recruitment of cortical structures during each task (Hanakawa et al., 2008). In general, kinesthetic imagery superior benefit to motor performance is due to a greater activation of neural regions related to motor activation compared to visual imagery (Guillot et al., 2014). Further, this form of MI has been reported to elicit greater corticospinal facilitation (Stinear et al., 2006a).
Here, we discuss to which extent MI and PP share overlapping neural substrates. Firstly, we will focus on the shared cortical and spinal activations between the two tasks.

CORTICAL OVERLAPPING ACTIVITY

PRIMARY MOTOR CORTEX

Since the major contribution by Jeannerod (2001), where the author reviewed experimental evidence that MI mirrors the preparation phase of actual motor performance at the cortical level, there has been a considerable increase of findings supporting the neurofunctional equivalence between MI and PP (for more recent reviews, see Lotze and Halsband, 2006, Munzert et al., 2009, Guillot et al., 2012a, Guillot et al., 2014, Ruffino et al., 2017). Methodologies such as functional magnetic resonance imagery (fMRI) and electroencephalography (EEG) have been largely adopted by researchers to better understand MI neurofunctional correlates. It is now well-accepted that MI and PP share overlapping substrates at the cerebral level, even though activation patterns are not strictly identical (See Figure 4). task. Main areas activated by motor imagery are: frontoparietal areas (mainly supplementary motor areas, ventral and dorsal premotor areas), frontal and temporal opercular areas, inferior parietal regions and cerebellum. Only a few areas of the premotor cortex and cerebellum were more active during more imagery than during physical practice. This figure was adapted from Hanakawa et al. (2008).
For instance, the primary motor cortex (M1) has been wildly reported as being active during MI. This region plays a critical role by sending the signals that control movements. Its activation during MI has been debated for a long time, since the first neuroimaging studies dealing with the mental simulation of actions (for a review, see Hétu et al., 2013). A pioneering study from Roland et al. (1980) using fMRI did not report activation of the contralateral M1 during MI. This finding was further supported by other studies which did not report M1 activation during MI (Binkofski et al., 2000, Gerardin et al., 2000, Hanakawa et al., 2003, Kuhtz􀇦 Buschbeck et al., 2003, Dechent et al., 2004, Hanakawa et al., 2008). At the meantime, a large amount of experiment using comparable methods to investigate the central nervous system activity reported peaks of activation in this region during MI (Leonardo et al., 1995, Sabbah et al., 1995, Porro et al., 1996, Roth et al., 1996, Lotze et al., 1999, Porro et al., 2000, Miyai et al., 2001, Ehrsson et al., 2003, Nair et al., 2003, Solodkin et al., 2004, Lacourse et al., 2005, Michelon et al., 2006, Guillot et al., 2008, 2009, Burianová et al., 2013).
Anatomically speaking, M1 can be divided into an anterior part, mainly of executive nature, and a posterior part, subserving primary cognitive functions (Sanes and Donoghue, 2000). Sharma et al. (2008) reported a smaller cluster distribution of the anterior part during MI compared to PP, while the posterior part had a similar activation between imagined and real task. Even with substantial literature attesting the activation of M1 during MI, an explanation to controversial data is required before adopting a conclusion. One important scientific consideration that may explain this inconsistent pattern of results is the temporal resolution of the technique used to map brain activations (Lotze and Halsband, 2006). Also, the MI modality is likely to elicit changes in the spatial distribution of cerebral activations. Kinesthetic MI is, for instance, known to induce greater M1 activation compared to visual imagery (Solodkin et al., 2004, Lorey et al., 2011, see Figure 4, adapted from Guillot et al., 2014 for visual representation of cortical activation during visual and kinesthetic imagery). Interestingly, Guillot et al. (2008) compared cortical activations of good imagers and poor imagers. To separate the groups, authors used an well-accepted questionnaire to evaluate MI ability (Hall and Martin, 1997), participants’ capacity to preserve temporal characteristics of the task during MI (Guillot et al., 2005a, Malouin et al., 2008) and electrodermal responses (Guillot and Collet, 2008) (All those parameters will be explained in details in following sessions). Authors reported brain activation differences between good and poor imagers, including selectively different M1 activity (see also Guillot et al., 2009, Lotze and Zentgraf, 2010). Kuhtz􀇦Buschbeck et al. (2003), combining fMRI and TMS measurements in complex vs simple imagined finger movements, reported an increased involvement of M1 during complex movements. This supports the postulate by Jackson et al. (2001), who argued that differently from PP, MI requires previous knowledge from task components by the participants before engaging in mental training (see also, Sharma et al., 2008, and Lotze and Zentgraf, 2010). To summarize, MI modality,
MI ability and task-knowledge might substantially influence M1 activation during mental representation. Despite such early controversial studies, the debate is somewhat resolved and there is now a growing consensus that M1 is active during MI.

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SECONDARY MOTOR AREAS

There is converging evidence that secondary motor areas, strongly involved in movement planning, programming and predicting, exhibit a comparable activity during PP and MI. Activation intensities observed during MI remain either lower (e.g., in the cerebellum, supplementary motor area and parietal operculum, Macuga and Frey, 2012) or higher (e.g., left superior frontal sulcus, bilateral superior precentral sulcus, superior frontal gyrus and right occipital cortex, Hanakawa et al., 2008), compared to PP. The overlap between PP and MI involves the following regions:
Ventral and dorsal premotor cortices: these regions have been extensively found to be active during imagined movements (see Lotze and Halsband, 2006, Guillot et al., 2008, Munzert et al., 2009). While the ventral part is responsible for cognitive aspects of action, the dorsal part is more related to movement preparation and execution (Rizzolatti et al., 1998). The ventral part was usually found to be more active during MI than during PP (Gerardin et al., 2000).
Supplementary Motor Area: This region is anatomically divided in three functional parts: i) the pre-SMA, involved in movement control, ii) the rostral part, involved in motor imagination, and iii) the caudal part, highly connected with motor execution (Vorobiev et al., 1998, Gerardin et al., 2000). Gerardin et al. (2000) reported two functional subdivisions for this area during MI, the post-SMA, where a rostro-caudal gradient was found between MI and PP, and the pre-SMA, more involved in imagination of the movement. While the SMA has punctually been emphasized for its role in the inhibition of M1 activity during MI (Kasess et al., 2008), its activation during imagined movements is well-admitted and systematically reported in the literature (Lotze et al., 1999, Hanakawa et al., 2003, Solodkin et al., 2004, Guillot et al., 2008, Olsson et al., 2008a, Guillot et al., 2009, Munzert et al., 2009).
Basal Ganglia: While this region is strongly involved in the storage of learned sequence movements and motor preparation (Alexander and Crutcher, 1990, Parent and Hazrati, 1995), there is now converging evidence of its activation during MI (see Gerardin et al., 2000, Nair et al., 2003, Lotze and Halsband, 2006, Guillot et al., 2008, Munzert et al., 2009), although little is known about its specific function (Guillot et al., 2014). Recently, Hanakawa et al. (2017) analyzed basal ganglia-cortical circuits during both PP and MI. When both tasks were completed in a faster pace, basal ganglia was more activated during PP and MI, compared with regular speed. Furthermore, due to the reduced activity observed in this regions in the Parkinson Disease group, authors concluded that basal ganglia may play a critical role in movement control during MI as well, through dopaminergic neurons.
Parietal Regions: Parietal regions include the somatosensory cortex and the parietal lobules (inferior and superior, as well as the precuneus). These areas were frequently found to be active during MI (see Lotze et al., 1999, Binkofski et al., 2000, Gerardin et al., 2000, Hanakawa et al., 2003, Nair et al., 2003, Guillot et al., 2009, Munzert et al., 2009). Lesions in the superior part of the parietal cortex is known to perturb the temporal congruence between MI and PP (Sirigu et al., 1996, Malouin et al., 2004, Sabaté et al., 2007), hence suggesting that this area would most likely be involved in planning processes during MI. In a seminal case-study, Schwoebel et al. (2002), asked a patient with bilateral parietal lesions to perform MI of hand movements. Surprisingly, the patient executed the movement during pure MI, without any awareness, thus demonstrating his incapacity to inhibit the motor command as usual. More recently, Kraeutner et al. (2016) induced a virtual “lesion” of the left inferior parietal lobule using continuous theta burst stimulation, and reported that intrinsic learning was impaired, therefore highlighting a disruption in MI-based skill acquisition.

Table of contents :

GENERAL INTRODUCTION
THEORETICAL FRAMEWORK I
I) MOTOR IMAGERY
A) DEFINITION
B) NEUROFUNCTIONAL BASES
(1) CORTICAL OVERLAPPING ACTIVITY
(i) PRIMARY MOTOR CORTEX
(ii) SECONDARY MOTOR AREAS
(2) CORTICOSPINAL EXCITABILITY FACILITATION
(i) SPECIFICITY OF CORTICOSPINAL RECRUITMENT DURING MOTOR IMAGERY
(ii) CORTICOSPINAL ACTIVATION THROUGH A PARALLEL PATH
(3) MOTOR INHIBITION DURING MOTOR IMAGERY
C) MOTOR IMAGERY ABILITY MEASUREMENT
(1) BEHAVIORAL MEASURES
(i) TEMPORAL CONGRUENCE
(ii) PSYCHOMETRIC MEASURES
(a) VIVIDNESS OF MOVEMENT IMAGERY QUESTIONNAIRE-2 (VMIQ-2)
(b) SELF-REPORT SUBJECTIVE MEASURES
(iii) PHYSIOLOGICAL MEASURES
(a) AUTONOMIC NERVOUS SYSTEM
􀁸 ELECTRODERMAL ACTIVITY
II) MENTAL REPRESENTATION AND PERFORMANCE
A) MENTAL REPRESENTATION DECOUPLED FROM ACTION
(1) SKILL PERFORMANCE AND LEARNING
(i) MOTOR IMAGERY EFFECT ON SKILL PERFORMANCE
(ii) MOTOR IMAGERY AND STRENGTH PERFORMANCE
(a) SPECIFICITIES OF MOTOR IMAGERY ON STRENGTH PERFORMANCE
B) MENTAL REPRESENTATION COMBINED WITH ACTION
(1) MENTAL REPRESENTATION ASSOCIATED WITH ACTION
(2) MENTAL REPRESENTATION INCLUDING ACTION
(3) MENTAL REPRESENTATION CONCOMITANT WITH ACTION EXPERIMENTAL PROCEDURES I
I) EFFECT OF MOTOR IMAGERY COMBINED WITH PRACTICE ON PERFORMANCE
EXPERIMENTAL CONTRIBUTION #1
EXPERIMENTAL CONTRIBUTION #2
THEORETICAL FRAMEWORK II
I) PSYCHOPHYSIOLOGICAL CORRELATES OF ACTION
A) PHYSICAL FATIGUE
B) FATIGUE MODELS
(1) CATASTROPHIC MODEL
(2) CENTRAL GOVERNOR MODEL
(i) CENTRAL NERVOUS SYSTEM AND FATIGUE
(a) NEURONAL FEEDBACK AND FATIGUE PERCEPTION
(3) PSYCHOBIOLOGICAL MODEL OF FATIGUE
C) PSYCHOPHYSIOLOGICAL MEASURES OF PHYSICAL FATIGUE
(1) CARDIORESPIRATORY MEASURES
(i) VENTILATORY AND ANAEROBIC THRESHOLD
(ii) VO2MAX MEASURE
(iii) HEART RATE
(2) SUBJECTIVE MEASURES
(i) RATE OF PERCEIVED EXERTION
EXPERIMENTAL PROCEDURES II
I) EFFECT OF FATIGUE ON MOTOR IMAGERY
EXPERIMENTAL CONTRIBUTION #3
EXPERIMENTAL CONTRIBUTION #4
II) EFFECT OF MOTOR IMAGERY DURING PRACTICE ON FATIGUE
EXPERIMENTAL CONTRIBUTION #5
EXPERIMENTAL CONTRIBUTION #6
GENERAL DISCUSSION
I) MOTOR IMAGERY PRACTICE CONCOMITANT TO ACTUAL TRAINING TO IMPROVE PERFORMANCE
II) THE EFFECTS OF FATIGUE PROCESSES ELICITED BY EXERCISE ON MOTOR IMAGERY ABILITY
III) USING MOTOR IMAGERY TO CONTROL DELETERIOUS EFFECTS OF FATIGUE ON PERFORMANCE
A) PRACTICAL RELEVANCE OF MOTOR IMAGERY PRACTICE IN THE PRESENCE OF FATIGUE
CONCLUSION
APPENDICES
BIBLIOGRAPHY

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