Study Provides New Insights Into The Functional Neuroanatomy Of Motor Imagery

April 1, 2003 (Bethesda, MD) -- Motor imagery has been extensively studied with positron emissions tomography (PET) and functional magnetic resonance imaging (fMRI) techniques. Converging evidence indicates that motor imagery shares neural substrates (substances changed by enzymes) with those underlying motor execution. However, less certain are how and to what extent neural substrates are shared between the two modes of motor-related behavior.

Background

The scientific community differs regarding involvement of the primary motor cortex (M1), the region of the cerebral cortex most nearly immediately influencing movements of the face, neck and trunk, and arm and leg, during motor imagery.  Some region-of-interest analyses from fMRI experiments often reveal mild activity increases in M1 during motor imagery, while group averaged analyses from fMRI and PET do not. 

Unfortunately, many of the fMRI studies showing M1 activity do not employ electrophysiological monitoring to exclude muscle contractions during actual scanning.  In addition to the methodological differences, there has been some diversity among the behavioral tasks studied as motor imagery. Motor imagery is defined as the mental simulation of a motor act. This definition can include various concepts such as preparation for movement, passive observations of action, and mental operations of sensorimotor representations, either implicitly or explicitly. Motor imagery as preparation for immediate movement likely involves the motor executive brain regions including M1, since M1 plays a significant role in sensory processing for the purpose of upcoming movement generation. Implicit mental operations of sensorimotor representations, on the other hand, are considered to underlie cognitive functions such as mental rotation of body parts. It is unclear whether a motor executive area such as M1 is active not only during motor preparation but also during mental operations of sensorimotor representations.

Another issue regarding neuroimaging studies on motor imagery is that the performance of imagination is notoriously difficult to control. To date, most studies have relied on subjective evaluation, rather than objective confirmation, of task performance. However, some neuroimaging studies on mental rotation or mental operations have successfully evaluated behavioral performance without involving any motor response during task periods. In these studies, subjects follow sensory stimuli given serially to update mental representations during the task, and then report the final image at the end of the task.

A New Study

In a new study, application of this task design allowed researchers to explore, for the first time, brain activity during explicit mental operations of finger representations with objective confirmation of performance. Specifically, specified times for a motor-imagery task were followed by a brief response period, during which subjects reported the final image of sensorimotor representation. This information was also used to explore brain areas associated with the task performance.  The authors of “Functional Properties of Brain Areas Associated with Motor Execution and Imagery,” are Takashi Hanakawa, Ilka Immisch, Keiichiro Toma, Michael A. Dimyan, Peter Van Gelderen, and Mark Hallett, all from the National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD. Their findings appear in the February 2003 edition of the Journal of Neurophysiology, one of 14 scientific journals published each month by the American Physiological Society (APS). 

Their research entailed using a fMRI to measure blood-oxygenation level-dependent changes as an index of neural activity. Performance during motor imagery was objectively confirmed by comparing sensory-guided execution of sequential finger tapping with mental operations of equivalent sensorimotor representations. To exclude possible muscle contractions during motor imagery and to capture them during motor execution and responses, muscle activity was electronically monitored during actual MRI acquisition.  Statistical parametric mapping revealed brain areas predominantly related to motor execution or motor imagery, and areas equally activated during both motor execution and imagery.

By capitalizing on relatively fine temporal resolution, sustained activity during the motor execution and imagery task compared with transient activity related to the response movement was also analyzed (time-course analysis). The time course analysis helped characterize the functional property of each set of areas from a different perspective, suggesting a functional gradation from more “executive” to more “imaginative” areas.

Methodology

Ten healthy volunteers [mean age, 32 + 11 (SD) years; seven males, three females] participated in this study. All were right handed and none had a history of any neuropsychiatric disorders.  Core elements of the research included:

• Number-Guided Segmented Sequential Finger Tapping Task. Subjects performed a finger-tapping task with their right hand in either a movement or an imagery mode of performance. Visually presented number stimuli (number 1, 2, or 3) that specified a segment of a finger tapping sequence guided the task throughout. For the movement mode, subjects actually executed the tapping movement as briskly and distinctly as possible. For the imagery mode, subjects were asked to imagine the corresponding tapping movement being performed by them (first person perspective) as opposed to the movement being performed by someone else, without any accompanying overt movement.

• Visual Fixation Task:  A visual fixation task was employed as a baseline condition for the fMRI experiment. Subjects were instructed to keep fixating on a cross that roughly matched the number stimuli in size and was presented for 750 ms at a rate of 0.67 Hz. During the visual fixation task, subjects were asked to clear their mind and withhold any movement except for physiological ones (i.e., natural blinking). 

• fMRI and electrophysiological monitoring:  The fMRI experiment was conducted on a 1.5-T GE/SIGNA scanner with a standard quadrature head coil. To reduce head motion during scanning, a bite bar made of a dental impression material was custom-made for each subject and fixed to a cradle of the head coil. Subjects lay supine on a scanner bed with a response device fixed to them at the wrist joint that had five buttons, one for each finger of the right hand. The subjects viewed visual stimuli back-projected onto a screen through a mirror built into the head coil, but were unable to see their hands during the fMRI experiment.

Results

The findings revealed that movement and imagery tasks were based on the same operational rules and stimuli, and obviously shared many processes.  These included visual information processing, conversion of the visual information to motor engrams according to arbitrary stimulus-response linkage, working memory, and monitoring instructed versus ongoing imagery/movement. Any mistake in these processes would result in failure to reach the correct answer for either task. The behavioral data, nevertheless, showed that the task performance was more accurate for the movement mode than for the imagery mode.

This suggested that different more than common components of the two modes affected the task performance. For the movement mode, the performance would rely primarily on motor control based on the somatosensory feedback in reference to the instructed movement. For the imagery mode, on the other hand, the task performance probably reflects success or failure in maintaining or upgrading mental finger representations in reference to the instructions.

For the difference in stimulus type, subjects tended to perform the tasks better for the fixed stimulus type than for the varied stimulus type that required higher stimulus dependency.  This might be especially true in the imagery mode for which subjects probably need more mental resources than for the movement mode, although this idea was not completely supported by the behavioral data (i.e., mode-by-stimulus interaction was not significant).

The results showed widespread response-related activity, reflecting many cognitive-motor processes involved in the button-press responses. This observation raises a concern about the ubiquitous assumption in neuroimaging experiments. This assumption is that subtraction of activity during a control sensorimotor task from activity during a cognitive task plus responses would reflect activity due to the cognitive task. However, such a subtraction may lead to false activation that merely reflects a difference between the complicated responses and simple movements because the response-related activity were widely present in the “nonmotor” areas including the dorsolateral prefrontal cortex.

Conclusions

The results provide evidence to support the concept of functional gradation from more imaginative properties to more motor executive properties in many cortical and subcortical areas. The most executive areas coincided with the motor areas that directly send output to M1 or the spinal cord or the areas associated with sensory feedback processing and somato-sensorimotor association.

However, some of the movement-predominant areas also showed imagery-related activity, supporting a functional gradation from imagery to movement. Many areas in the frontoparietal cortex and posterolateral cerebellum showed similar activity between the movement and imagery modes that share multiple components of the tasks.   The areas most active with imagery (PcS/MFG, precuneus) may reflect a requirement of motor inhibition or attention to hand-centered space. The left frontoparietal areas correlated with the imagery task performance can be considered the primary basis of sensory-guided motor imagery studied in the present study. Finally, the effect of stimulus variability on motor imagery was observed in the inferior precentral sulcus, suggesting importance of the matching system between the ongoing and the instructed behavior.

Source: February 2003 edition of the Journal of Neurophysiology, one of 14 scientific journals published each month by the American Physiological Society (APS). 

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The American Physiological Society (APS) was founded in 1887 to foster basic and applied science, much of it relating to human health. The Bethesda, MD-based Society has more than 10,000 members and publishes 3,800 articles in its 14 peer-reviewed journals every year.

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Editor’s Note: To set up an interview with a member of the research team, please contact Donna Krupa at 703.527.7357 (direct dial), 703.967.2751 (cell) or djkrupa1@aol.com.