Elsevier

NeuroImage

Volume 42, Issue 1, 1 August 2008, Pages 343-356
NeuroImage

Functional neuroimaging correlates of finger-tapping task variations: An ALE meta-analysis

https://doi.org/10.1016/j.neuroimage.2008.04.025Get rights and content

Abstract

Finger-tapping tasks are one of the most common paradigms used to study the human motor system in functional neuroimaging studies. These tasks can vary both in the presence or absence of a pacing stimulus as well as in the complexity of the tapping task. A voxel-wise, coordinate-based meta-analysis was performed on 685 sets of activation foci in Talairach space gathered from 38 published studies employing finger-tapping tasks. Clusters of concordance were identified within the primary sensorimotor cortices, supplementary motor area, premotor cortex, inferior parietal cortices, basal ganglia, and anterior cerebellum. Subsequent analyses performed on subsets of the primary set of foci demonstrated that the use of a pacing stimulus resulted in a larger, more diverse network of concordance clusters, in comparison to varying the complexity of the tapping task. The majority of the additional concordance clusters occurred in regions involved in the temporal aspects of the tapping task, rather than its execution. Tapping tasks employing a visual pacing stimulus recruited a set of nodes distinct from the results observed in those tasks employing either an auditory or no pacing stimulus, suggesting differing cognitive networks when integrating visual or auditory pacing stimuli into simple motor tasks. The relatively uniform network of concordance clusters observed across the more complex finger-tapping tasks suggests that further complexity, beyond the use of multi-finger sequences or bimanual tasks, may be required to fully reveal those brain regions necessary to execute truly complex movements.

Introduction

Finger-tapping tasks are commonly used to study the human motor system in functional neuroimaging studies. Tapping tasks have the advantage of being simple enough to use in the study of both normal control subjects as well as those with neuropathologies affecting the motor system, while being flexible enough to accommodate numerous modifications. These tasks can vary across studies both by the use or lack of a pacing stimulus and in the relative complexity of the tapping task.

Pacing stimuli are used to ensure that all subjects uniformly perform a given finger-tapping task at a predetermined rate. The stimuli are usually in the form of a regularly paced, repetitive auditory or visual cue, such as that produced by a metronome (e.g. Catalan et al., 1998, Colebatch et al., 1991, Sadato et al., 1996a) or blinking light (e.g. Indovina and Sanes, 2001, Jäncke et al., 2000b), respectively. Such finger-tapping tasks performed in the presence of a pacing stimulus are referred to as externally guided or externally generated. In contrast, the task can be performed in the absence of any pacing stimulus (i.e. self-paced). Such self-paced tapping tasks are referred to as internally guided or internally generated. The results from studies investigating the effects of auditory and visual pacing stimuli have reported different networks of active brain regions, however, these results are not consistent across different studies.

Pacing stimuli are also often used in conjunction with more complex finger-tapping tasks such as multi-finger sequential or bimanual tapping tasks. For the purposes of the ensuing analyses, multi-finger sequential tapping tasks were taken to be complex in terms of the increased number of fingers involved in the task; factors such as the rate of movement and the length of the sequence were not specifically considered. Bimanual tasks were taken to be any task involving the tapping of fingers on both hands, regardless of the symmetry. These types of complex finger-tapping tasks are often employed to elicit neural activation that is more representative of what would be observed in typical, everyday manual movements that may not be practical to complete within the confines of a MRI or PET scanner. The use of complex finger-tapping tasks also allows for the further study of secondary and tertiary neural motor regions that may not be active during a simple, unimanual index finger-tapping task.

Results from studies employing finger-tapping tasks can be divergent due to variations in the experimental paradigms used, making them difficult to interpret across studies. Additionally, studies can choose to focus on a few specific neural regions (e.g. Jäncke et al., 2000a, Colebatch et al., 1991, De Luca et al., 2005), resulting in partial descriptions of the underlying neural network involved in a given tapping task. A quantitative meta-analysis technique, such as that proposed independently by Turkeltaub et al. (2002) and Chein et al. (2002) provides a method to assess the degree of concordance across multiple studies. The results of such an analysis can be useful in determining a more complete network of neural regions involved in a given task or paradigm as well as in forming new hypotheses and interpreting results from subjects with neurological impairments.

This present study was not the first to use quantitative meta-analysis techniques to assess concordance across studies examining the human motor system. Chouinard and Paus (2006) employed a similar technique to further elucidate the roles of the primary motor and premotor cortices in various motor tasks. Four motor-related tasks – movement response selection, movement response to a stimulus, execution of object-related hand movements, and observation of object-related hand movements – were chosen to map out the roles of the dorsal and ventral premotor cortices in these tasks. Chouinard and Paus were successful in utilizing meta-analysis to identify several distinct nonprimary motor areas within the motor cortex.

In the present meta-analysis, our aim was to isolate the corpus of published literature for simple hand movements (i.e., finger tapping), and identify the entire network of brain regions associated with this type of motor task. Our intent was to examine agreement across studies not only in the motor cortex, but also throughout all cortical, subcortical, and cerebellar regions. In addition, meta-analysis was used to differentiate the brain regions that are active during the most common variations of finger-tapping tasks: auditorially-paced, visually-paced, self-paced, single index finger, unimanual, dominant hand (RH) multi-finger sequence, and bimanual, as well as to compare these networks among the tapping task variations. We hypothesized that the choice of finger-tapping task variation would have a strong influence on the observed network of active brain regions.

Section snippets

Methods

Several literature searches were performed in Medline to find the published corpus of literature prior to July 2006 involving finger-tapping tasks in unimpaired, right-handed subjects. References from all relevant papers were also examined. From these search results, only those papers which reported activations as coordinates in stereotactic space (x,y,z) were considered. Papers directly addressing motor learning or using over-trained subjects such as professional musicians were excluded.

Results

The ALE map for the main effects of all finger-tapping task variations included in this study is shown in Fig. 1. Common, robust concordance was seen in bilateral sensorimotor cortices (L: − 38,− 26,50; R: 36,− 22,54), supplementary motor area (SMA) (− 4,− 8,52), left ventral premotor cortex (− 54,− 2,32), bilateral inferior parietal cortices (L: − 50,− 26,20; R: 40,− 42,44), bilateral basal ganglia (L: − 22,− 8,4; R: 22,− 10,6), and bilateral anterior cerebellum (L: − 22,− 52,22; R: 16,− 50,− 20). Smaller

Discussion

An ALE meta-analysis was performed to quantify the motor system during finger tapping, a common task used in functional imaging studies. Results allowed for detailed description of the motor networks involved in single finger, unimanual, dominant hand multi-finger, and bimanual movement sequences, varying in the presence or absence of a pacing (auditory or visual) stimulus.

Conclusions

From the results of the meta-analyses performed, it appears that the choice or lack of a pacing stimulus has a greater effect on the network of brain regions consistently reported to be active than the choice of a more complex tapping task. For all of the task variations considered, though, the additional regions reported to be active, beyond those involved in the general motor execution, seem to be involved preferentially in the temporal aspects of the tapping task. The use of a visual pacing

Acknowledgments

ARL was supported by the Human Brain Project of the NIMH (R01-MH074457-01A1; PI: Peter T. Fox). STW was supported by the Vilas (William F) Trust Estate: Vilas Life Cycle Professorship and NIH (R01-CA118365-01; PI: M. Elizabeth Meyerand).

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