Cortical and cerebellar activity of the human brain during imagined and executed unimanual and bimanual action sequences: a functional MRI study

Abstract

The neural (blood oxygenation level dependent) correlates of executed and imagined finger sequences, both unimanual and bimanual, were studied in adult right-handed volunteers using functional magnetic resonance imaging (fMRI) of the entire brain. The finger to thumb opposition tasks each consisted of three conditions, two unimanual and one bimanual. Each experimental condition consisted of overt movement of the fingers in a prescribed sequence and imagery of the same task. An intricate network consisting of sensorimotor cortex, supplementary motor area (SMA), superior parietal lobule and cerebellum was identified when the tasks involved both planning and execution. During imagery alone, however, cerebellar activity was largely absent. This apparent decoupling of sensorimotor cortical and cerebellar areas during imagined movement sequences, suggests that cortico-cerebellar loops are engaged only when action sequences are both intended and realized. In line with recent models of motor control, the cerebellum may monitor cortical output and feed back corrective information to the motor cortex primarily during actual, not imagined, movements. Although parietal cortex activation occurred during both execution and imagery tasks, it was most consistently present during bimanual action sequences. The engagement of the superior parietal lobule appears to be related to the increased attention and memory resources associated, in the present instance, with coordinating difficult bimanual sequences.

Introduction

Understanding the neural correlates of goal-directed action, whether executed or imagined, has been an important domain of cognitive brain research since the advent of functional imaging studies using positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) [17], [27], [28], [29], [31], [34], [38], [41]. A majority of studies has focused on the activation of individual brain areas, such as the sensorimotor cortex, the supplementary motor area (SMA) or the cerebellum. In this study, using fMRI of the entire brain, we aim to furnish a more complete view of brain activation during finger-sequencing tasks. We compare brain activation during overt and imagined movements, both unimanual (left and right hand separately) and bimanual (both hands sequencing together).

A complex movement task such as sequential finger movement involves many processes, including movement planning, selection, prediction and execution, whereas imagery of the same task requires the same set of processes, except the last. Due to this inherent difference in the nature of the two tasks, one should expect differences in brain activation. The question of whether motor execution and imagery share common neural resources has been addressed by many studies in the recent past. Significant increases in fMRI signal intensity were observed in the pre-central (primary motor cortex, M1) and the post-central gyri (primary somatosensory cortex, S1), during both motor performance and imagery of a finger-to-thumb opposition task [31]. The same task induced activation in contralateral M1, S1 and pre-motor cortices during actual execution but only in M1 and premotor cortex during mental simulation in another study [34]. When subjects were asked to make fists and then imagine doing the same, increased fMRI signal intensity was observed in M1, premotor cortex and the SMA during both execution and imagery tasks, with S1 showing significantly less activation during imagery [27]. Cerebral blood flow measured using PET was observed to increase in medial and lateral premotor areas as well as cingulate motor area (CMA) during both execution and imagery of joystick movements [38]. The latter study also reported additional activation in primary sensorimotor cortex and rostral superior parietal lobe during task execution [38]. Compared to actual motor performance, imagery appears to produce significantly lower fMRI signal changes in the cerebellum [27], [28]. Although these studies used different tasks (making fists [27] and finger to thumb opposition [28]), both reported differential activation of the cerebellum during execution and imagery: strong activation of the anterior cerebellum was observed during execution while imagery resulted in posterior lobe activation. Movement execution thus seems to engage a large network of brain areas including the M1, S1, premotor areas (SMA, CMA), superior parietal lobule and the cerebellum. Imagery of the same movements seems to engage almost all these areas, although the intensity of activation appears to drop off in S1 and cerebellum.

Unimanual and bimanual tasks employ overlapping as well as different neural resources [13]. In right-handed individuals, the right sensorimotor cortex was found to be more active than the left in unimanual finger sequencing tasks, whereas the left showed more activation than the right sensorimotor cortex during bimanual tasks [13]. For both unimanual and bimanual tasks, the area and intensity of brain activation appear to increase with task complexity, force and rate of movement [13], [14], [32], [33], [35], [36], [40], [42]. SMA, pre-SMA and CMA have been implicated in the control of complex finger movements [5], [6], [15], [25], [36]. Comparing repetitive tapping of the index finger with sequential movement of fingers, Wexler et al. [42], found that the parietal lobe, especially the superior parietal area, was selectively activated in the more complex finger-sequencing task. In self-paced finger movements, however, cortical structures around the intra-parietal sulcus were activated [35]. The intra-parietal sulcus is also active when finger movements are coordinated with reference to a specific spatial reference [1], [16]. It appears that the parietal cortex is involved in a wide variety of tasks, especially those in which subjects need to access spatial information and spatial memory. Since unimanual and bimanual tasks basically differ in the involvement of one versus two hemispheres, studies have focused on the laterality of brain activation during such tasks. In right-handed individuals, significant ipsilateral (left) motor cortex (M1) activation is observed during movement with the non-preferred (left) hand [25], [37]. Such ipsilateral activation for movement of the non-dominant hand has been attributed to task complexity [33]. Similarly, some studies have reported bilateral cerebellar activation when right-handed subjects moved using their non-dominant left hand [8], [14]. These findings suggest that when subjects perform tasks with their non-dominant hand, an additional neural loop consisting of motor areas of both the hemispheres is involved, that facilitates coordination of motor behavior.

In the present study, we aim to identify the brain areas involved in both overt finger sequencing and imagery alone conditions. Following Jäncke et al. [13] we studied differences in brain activation between unimanual and bimanual finger movements. Here, however, instead of using a simple finger-sequencing (2345) task, a different movement sequence was prescribed for each task (left, right and bimanual conditions) in order to minimize or at least balance effects due to learning, and to control for task difficulty across exemplars of the task. By imaging the entire brain during these tasks, our main goals were 2-fold: first, to understand how cortical and cerebellar areas are differentially engaged during the course of motor performance and imagery. In particular, we expected on the basis of older [22] and more recent models of motor control [43] which posit extensive internal feedback and feedforward cerebro-cerebellar loops, that cerebellar involvement will be greater during active, planned than imagined movement sequences. This is because of the putative role of the cerebellum in correcting errors in motor commands prior to their effects at the periphery. Our second goal was to clarify the role of parietal and other cortical areas in movements such as complex bimanual action sequences, which incorporate spatial information and spatial memory. In particular, evidence from patients with parietal lesions suggests frank motor imagery deficits [4], [18]. On this basis, we might expect greater parietal involvement as the task becomes more difficult to imagine, such as when the non-preferred hand is used or when both hands are sequencing together.