Effector-independent brain activity during motor imagery of the upper and lower limbs: An fMRI study

Neuroscience Letters 581 (2014) 69–74

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Effector-independent brain activity during motor imagery of the upper and lower limbs: An fMRI study Nobuaki Mizuguchi ∗ , Hiroki Nakata, Kazuyuki Kanosue Faculty of Sport Sciences, Waseda University, 2-579-15 Mikajima, Tokorozawa, Saitama, 359-1192, Japan

h i g h l i g h t s • Brain activity was measured by functional magnetic resonance imaging. • We evaluated the common brain region of motor imagery of the right/left hands or feet. • The left supplemental motor area and inferior frontal gyrus were commonly activated.

a r t i c l e

i n f o

Article history: Received 16 June 2014 Received in revised form 23 July 2014 Accepted 13 August 2014 Available online 20 August 2014 Keywords: Mental practice Hand Foot Area 44 Supplemental motor area

a b s t r a c t We utilized functional magnetic resonance imaging (fMRI) to evaluate the common brain region of motor imagery for the right and left upper and lower limbs. The subjects were instructed to repeatedly imagined extension and flexion of the right or left hands/ankles. Brain regions, which included the supplemental motor area (SMA), premotor cortex and parietal cortex, were activated during motor imagery. Conjunction analysis revealed that the left SMA and inferior frontal gyrus (IFG)/ventral premotor cortex (vPM) were commonly activated with motor imagery of the right hand, left hand, right foot, and left foot. This result suggests that these brain regions are activated during motor imagery in an effector independent manner. © 2014 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Motor imagery is a mental process that involves the simulation of motor execution [25]. Many studies have reported significant effects of motor imagery practice on improvement of motor skill, muscle strength and joint flexibility [11,17,31,34,47]. In addition, motor imagery has been utilized to create a brain computer interface [37]. Neuroimaging studies using functional magnetic resonance imaging (fMRI) have demonstrated that various regions such as the supplemental motor area (SMA), the premotor cortex (PM), the parietal region, the basal ganglia and the cerebellum are activated during motor imagery [7,8,16,19,20,29,30,32,33,36]. Previous studies also report that brain activity during motor imagery largely overlaps activity that occurs during actual motor execution [16,19,20,30,31]. A previous study suggested that a hierarchy exists in the action representation (i.e. effector dependent and effector independent manner) [23]. We consider that clarifying

∗ Corresponding author. Tel.: +81 4 2947 6826; fax: +81 4 2947 6826. E-mail address: [email protected] (N. Mizuguchi). http://dx.doi.org/10.1016/j.neulet.2014.08.025 0304-3940/© 2014 Elsevier Ireland Ltd. All rights reserved.

effector-independent activity during motor imagery would give important information to understand the neural mechanisms underlying higher order action representation in motor imagery. Several studies have found activation of the left inferior frontal gyrus (IFG)/ventral PM (vPM) during voluntary hand movements. This activation is independent of hand side [41]. For example, Heim et al. report that the left IFG and SMA were commonly activated not only during right and left hand movements, but also during speech [21]. In addition, patients with a stroke in the left hemisphere exhibited impaired voluntary movements of both right and left hands [18]. Therefore, motor-related brain regions in the left hemisphere would have an important role in motor execution irrespective of the side of the activated hand. Activity in the left PM was also observed during action planning and motor imagery [1,2]. For example, the left frontal operculum (Brodmann area: BA 44) and the SMA were activated during imagery involving both right and left hand unimanual movements [1]. The left PM is also activated during voluntary foot movements [5]. A previous study reported that the left vPM was activated during imagery of the right lower limb movement [45]. A recent meta-analysis demonstrated that brain activity during upper and

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lower limb movement was observed in the front-parietal regions including the left IFG [22]. However, since this meta-analysis did not address the independence of the right and left limbs, it remains unclear as to whether the left IFG was commonly activated during motor imagery of right and left foot movement. Swinnen and colleagues demonstrated that the left IFG/vPM and parietal regions are activated during both right and left hand-foot coordination movements. This suggests that the left parietal-premotor areas are candidates for effector-independent movement encoding as the highest level in the action representation hierarchy [43]. The overall conclusion gleaned from the above studies is that the left IFG/vPM plays an important role in both motor execution and imagery, irrespective of hand or foot side. This leads to the supposition that the left IFG/vPM is a viable candidate for the structure encoding motor imagery in an effector-independent manner, since the loci of increased brain activity during motor execution and motor imagery are similar [10]. To date, no studies have examined whether the left IFG/vPM is commonly activated during motor imagery of the right/left hands or feet. To evaluate the above hypothesis, the present study utilized fMRI, and measured the blood oxygenation level-dependent (BOLD) signal to evaluate the common brain regions activated by motor imagery of the right and left as well as the upper and lower limbs. A previous study demonstrated that the modality of explicit imagery (i.e. kinesthetic and visual imagery) affects brain activity [16]. In the present study, we investigated brain activity during kinesthetic motor imagery. We hypothesized that activity in the left IFG/vPM would be commonly observed among the four imagery conditions (i.e. right hand, left hand, right foot, and left foot).

2. Methods and materials 2.1. Subjects Seventeen normal subjects (one female and 16 males; mean age 23.3 ± 2.5 years) participated in this study. All subjects were undergraduate or graduate students. All of them were right-handed according to the Edinburgh Inventory [38], and right-footed according to Chapman’s Footedness Test [6]. The subjects had no history of neurological or psychiatric disorders. Before the experiment, written informed consent was obtained from all subjects. The study was approved by the Human Research Ethics committee of the Faculty of Sport Sciences, Waseda University.

2.2. Procedure The subjects performed four motor imagery tasks: (1) right hand imagery (RH), (2) left hand imagery (LH), (3) right foot imagery (RF) and (4) left foot imagery (LF). In the RH and LH tasks, the subjects were asked to repeatedly imagine extension and flexion of the right or left hand. In the RF and LF tasks, the subjects were instructed to repeatedly imagine plantar flexion and dorsiflexion of the right or left ankle. Before the fMRI scan, differences in motor imagery between kinesthetic and visual imagery were explained to the subjects. The subjects were instructed to perform the imaging of the movements with a comfortable, self-paced rhythm utilizing kinesthetic imagery and to keep the same rhythm among the four conditions. A practice session with several trials of motor imagery including extension and flexion was performed before the recording to enable the subjects to become familiar with the situation. After recording each condition, we verbally asked the subjects whether motor imagery with the same rhythm could be successfully performed. It was confirmed that all subjects performed clear motor imagery in all conditions.

For the MRI scans, a 5 min 12 s run for each condition consisted of five alternate repetitions of the task and a rest period. The durations of the task and the rest periods were both 30 s. The first four volumes (12 s) of each fMRI session were discarded because of unstable magnetization. The subjects were presented with a blue-filled or red-filled circle cue via a PC controlled projector system (VisuaStimDigital, Resonance Technology Co., USA). The circles were presented with a black background and were viewed through non-magnetic goggles. When the blue cue was presented, the subjects were instructed to mentally reproduce the requested limb movement without any muscle activation. When the red cue was shown, the subjects were asked to relax and to not image. The subjects were also asked to keep their muscles relaxed and not to think about anything throughout the entire procedure. Any communication between the experimenter and the subject was made via intercom. 2.3. fMRI data acquisition and analysis All images were acquired using a 1.5 T MR scanner (Signa, General Electric, Wisc., USA). BOLD contrast functional images were acquired using T2*-weighted echo planar imaging (EPI) free induction decay (FID) sequences with the following parameters: TR 3000 ms, TE 50 ms, FOV 22 cm × 22 cm, flip angle 90◦ , slice thickness 5 mm and gap 1 mm. The orientation of the axial slices was parallel to the AC–PC line. For anatomical reference, T1-weighted images (TR 30 ms, TE 6 ms, FOV 24 cm × 24 cm, flip angle 90◦ , slice thickness 1 mm and no gap) were also obtained for each subject. The raw data were analyzed with a Statistical Parametric Mapping (SPM8, Wellcome Department of Cognitive Neurology, London, UK) [12–14] program implemented in MATLAB (Mathworks, Sherborn, Massachusetts, USA). Realigned images were normalized to the standard space of the Montreal Neurological Institute brain (MNI brain). Subsequently, smoothing was executed with an isotropic three-dimensional Gaussian filter with full-width at a half-maximum (FWHM) of 8 mm. High-pass filters (128 s) were also applied and low frequency noise and global changes in the signals were removed. Statistical analysis was performed on two levels. The first-level analysis performed for each subject was done with the general linear model. We constructed a statistical parametric map of the t-statistic for each of the four contrasts; (1) RH, (2) LH, (3) RF, and (4) LF. Subject-specific contrast images of the estimated parameter were used for the second-level analysis (random-effect model) [15]. The second-level analysis utilizing a full factorial design (oneway ANOVA, factor = limb, four levels) was performed to extend the inference of individual activation data to the general population. A conjunction analysis was also employed in order to detect brain regions activated commonly in all four conditions utilizing SPM8 [39]. Anatomical locations and Brodmann’s areas were determined utilizing the anatomy tool box (version 1.8) of SPM. The statistical threshold was set at p < 0.001 uncorrected (spatial extent > 10 voxels) [24]. If significant activation was evaluated as ‘Not found in any probability map’, it was excluded from description in the results section as well as in the tables. 3. Results Brain activities related to RH imaging were located in the left SMA (BA 6), rolandic operculum (BA 44), and primary somatosensory cortex (S1) (BA 1). In the right hemisphere, activation was observed in the PM (BA 6) (Fig. 1, Table 1). Regions activated by LH imaging were located in the left SMA (BA 6), PM (BA 6), IFG (BA 44), pallidum, amygdala, caudate nucleus, and cerebellum. The activities in the right hemisphere were seen in the PM (BA 6), rolandic

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Table 1 Activated regions during motor imagery of the right/left hands/feet. Region

Right hand Supplementary motor area Precentral gyrus Rolandic operculum Precentral gyrus Middle frontal gyrus Postcentral gyrus Supra marginal gyrus Superior parietal lobule Superior parietal lobule Insula lobe Hippocampus Middle temporal gyrus Left hand Supplementary motor area Precentral gyrus Middle frontal gyrus Precentral gyrus Inferior frontal gyrus Rolandic operculum Inferior frontal gyrus Superior frontal gyrus Precentral gyrus Rolandic operculim Inferior frontal gyrus Supra marginal gyrus Inferior parietal lobule Inferior parietal lobule Postcentral gyrus Inferior parietal lobule Middle temporal gyrus Inferior temporal gyrus Superior temporal gyrus Putamen Pallidum Amygdala Insula lobe Caudate nucleus Olfactory cortex Cerebellum Cerebellum Right foot Supplementary motor area Inferior frontal gyrus Supra marginal gyrus Left foot Inferior frontal gyrus Inferior frontal gyrus Inferior frontal gyrus Inferior frontal gyrus Middle frontal gyrus Supplementary motor area Superior frontal gyrus

Side

BA

L L L R L L L L R R L R

6 44 44 6 6

L L L L R R L R R L L L L L R R L L R R L L R L R L R

6

L L L

6 44

R R L L L L L

1

6 44

6 44

3a

Lobule VI Lobule VI

44 44 6

operculum (BA 44), S1 (BA 3a), putamen, insula, olfactory cortex, and cerebellum (Fig. 1, Table 1). Activated regions in the RF were shown in the left SMA (BA 6) and IFG (BA 44) (Fig. 1, Table 1). Brain activities related to the LF were located in the left SMA (BA 6), IFG (BA 44), and right IFG (BA 44) (Fig. 1, Table 1). Conjunction analysis for common regions activated in the RH, LH, RF, and LF conditions revealed significant activation in the left SMA (BA 6) and IFG/vPM (BA 44) (Fig. 2, Table 2). 4. Discussion We observed activation in one or more of the four conditions for a number of brain regions including the SMA, PM, IFG/vPM (area 44), and S1. This result is consistent with the results of previous neuroimaging studies examining motor imagery [16,19,20,30,31,35]. Conjunction analysis revealed that the left SMA

Z-score

MNI coodinates X

Y

Z

−10 −56 −56 58 −42 −52 −58 −28 58 44 −18 64

4 4 4 8 4 −22 −36 −46 −30 6 −8 −50

68 22 12 36 56 26 28 70 24 2 −14 −2

4.52 4.50 4.30 3.60 3.45 3.58 4.03 3.55 3.40 3.74 3.70 3.18

−6 −46 −26 −42 62 62 −36 28 36 −48 −60 −54 −52 −36 34 60 −50 −50 58 26 −24 −20 26 −4 4 −8 10

8 6 4 −6 12 10 34 −4 −10 6 8 −38 −44 −44 −30 −38 −38 −46 −36 0 −8 −4 20 10 12 −64 −66

54 50 50 44 20 6 −8 68 52 2 10 30 44 40 40 46 −14 −8 20 2 −2 −12 −18 −2 −4 −12 −14

5.27 5.29 4.60 4.21 4.19 4.14 3.75 3.73 3.59 5.12 3.83 4.28 4.08 3.28 3.50 3.92 3.58 3.53 3.70 4.11 3.59 3.29 3.45 3.40 3.12 4.81 3.80

−8 −46 −52

0 4 −34

60 4 24

4.22 3.51 3.28

60 62 −46 −58 −48 −8 −24

16 14 6 10 8 0 4

34 26 8 16 52 60 64

4.27 4.25 3.76 3.17 3.75 3.65 3.27

and IFG/vPM were commonly activated during motor imagery irrespective which of the four limbs was imaged. An additional analysis revealed that activity in the left SMA and IFG/PMv did not differ among conditions (see supplementary material). This result implies that these regions have a similar function in motor imagery irrespective of limbs or laterality. This finding suggests that the left SMA

Table 2 Activated regions identified by conjunction analysis. Region

Side BA

Supplementary motor area Inferior frontal gyrus

L L

6 44

MNI coodinates X

Y

Z

−8 −46

0 4

60 4

Z-score

3.65 3.51

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Fig. 2. Brain regions commonly activated in right hand, left hand, right foot and left foot imaging. Active neural sites are superimposed on the MNI standard brain.

Fig. 1. Activated regions during motor imagery utilizing the right hand (RH), left hand (LH), right foot (RF) and left foot (LF), respectively. Activities are superimposed on the MNI standard brain.

were activated during motor imagery irrespective of upper or lower limbs [22]. This difference was likely caused by the difference of statistical power between the present study and the meta-analysis. That is, if we increased the number of subjects, we might have been able to detect such brain activity. Anatomically, area 44 in the IFG corresponded to the F5 in nonhuman primates [2]. F5 neurons encoded specific motor acts such as grasping, irrespective of which hand was involved [40]. Therefore, area 44 in the IFG is likely to generate goal directed motor commands which are relayed to the primary motor cortex (M1). A human study supports this notion. Manipulation of complex objects such as plastic toys activates the IFG/vPM (area 44) [3]. Taken together, activity in the left IFG/vPM, during motor imagery would be related to motor planning of the intended movement rather than motor control. In the present study, the left IFG/vPM might encode repetitive extension and flexion of a limb during motor imagery, irrespective of limbs. 4.2. SMA

and IFG/vPM play important roles in motor imagery in an effector independent manner. 4.1. IFG/vPM A previous study found that the IFG (area 44) was commonly activated during imagery of either the right or left hand [1]. The left vPM was also activated during imagery of the right lower limb movement [45]. In addition, a meta-analysis that there was activity in the left IFG/vPM during motor imagery of the upper and lower limbs [22]. Our results confirmed these findings that the left IFG/vPM was activated during imagery utilizing both hands and feet, and furthermore provided new evidence regarding the common neural substrate of motor imagery. However, the metaanalysis demonstrated that not only the left IFG/vPM and SMA but also the superior parietal lobule, putamen, insula, and cerebellum

As for the role of the SMA in the neural networks involved with motor imagery, an inhibitory function in the execution of voluntary movements could well be involved. Kasess et al. examined effective connectivity between the SMA and M1 during motor imagery. They utilized dynamic causal modeling, and suggested that the SMA suppressed activity in the M1 during motor imagery [27]. The study by Kasess et al. implies that activity in the SMA is needed to insure that no muscle activity occurs during motor imagery. However, their study only investigated the effective connectivity between the SMA and M1. A recent MEG study also suggests that the activity in the SMA inhibits the activity in M1 as assessed by MEG beta (13–35 Hz) signals during motor imagery [9]. This study investigated SMA and M1 activity during motor imagery which was recorded from a quadriplegic patient. They found that higher activity in M1 and lower activity in SMA were observed during motor

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imagery as compared that observed in healthy subjects. This indicates that inhibition from SMA to M1 was impaired during motor imagery in the quadriplegic patients probably because the patients need not to inhibit muscle contraction or M1 activity during motor imagery. In the present study, we were unable to address the issue for function of the SMA during motor imagery, but according to fMRI and MEG findings, we speculate that activity in the SMA suppressed activity in the M1, in order to insure that muscle contraction was not generated during motor imagery. Indeed a strong neuroanatomical connection exists between the SMA and M1 [26]. We also hypothesized that inhibition from SMA to M1 is not limb specific. This is because the inhibitory signals suppress not only effector muscles of motor imagery but also non-effector muscles [28]. In one example, Tabu et al. report common activation during both hand and foot stop signal paradigms that were proposed to emanate from the pre SMA [44].

4.3. Limitation In the present study, we set the threshold at p < 0.001 uncorrected. This threshold was relatively liberal compared to corrected threshold such as the familywise error rate. Therefore, our findings might contain false positives. However, brain activity in the left IFG/vPM and SMA during motor imagery was consistent with previous studies [22,41]. Therefore, we believe that the left IFG/vPM and SMA have an important role in motor imagery independent of effectors. Although we did not record an electromyogram for each muscle during motor imagery in the fMRI scan, the lack of M1 activation would indicate that actual muscle activity was minimal or absent during the motor imagery tasks. Therefore, brain activity in the present study would reflect motor imagery but not intended or unintended muscle activity. We were not able to confirm whether the subjects’ rhythms were exactly the same through the experiment. Therefore, the self-paced rhythm might have differed among conditions. In addition, in the present study, 16 of the 17 subjects were male. A previous study reported that a gender difference was observed in brain activity during a mental rotation task [42]. Furthermore, since motor imagery ability would affect brain activity during motor imagery [46], we did not record motor imagery ability. In the future, we need to clarify whether effector-independent activity during motor imagery was different between male and female subjects or was affected by motor imagery ability.

5. Conclusion In conclusion, in this study we demonstrated that the left SMA and IFG/vPM exhibit effector-independent activity during motor imagery. These regions are thus likely to have an important role in higher order action representation during motor imagery. This new information will be helpful for understanding the neural mechanisms underlying motor imagery.

Acknowledgments The authors thank Dr. Larry Crawshaw for English editing. This work was supported by JSPS KAKENHI grant number 24800092 and Grant-in-Aid from the Global COE “Sport Sciences for the Promotion of Active Life”, Waseda University, from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.neulet. 2014.08.025.

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