Elsevier

NeuroImage

Volume 39, Issue 2, 15 January 2008, Pages 825-831
NeuroImage

Cervical spinal cord BOLD fMRI study: Modulation of functional activation by dexterity of dominant and non-dominant hands

https://doi.org/10.1016/j.neuroimage.2007.09.026Get rights and content

Abstract

The objective of this study was to investigate the effect of dexterity on the magnitude of signal changes in functional magnetic resonance imaging (fMRI) in the cervical spinal cord with unilateral finger-tapping. Right-handed healthy volunteers were investigated with blood oxygenation level-dependent (BOLD) fMRI. Spinal cord BOLD functional MR images were acquired from 10 healthy right-handed volunteers who performed four sessions of unilateral finger-tapping tasks: left sequential (LS), right sequential (RS), left interleaved (LI), and right interleaved (RI) tasks. Our results from the difficulty measurement test showed that finger-tapping in interleaved order was more difficult than in sequential order. For the functional activation, seven out of 10 subjects had activation in all four fMRI sessions (two of the subjects who showed no detectable activation had problems in volume registration). The mean contrast value of the activation area inside the entire cervical spinal cord was significantly higher in performing LS than RS tasks. The increase in the mean contrast value was because the less skilled and competent right hemisphere required additional processing power for doing the left hand task than the left hemisphere required in doing the right hand task. The analysis of the interleaved finger-tapping tasks did not show any significant difference in the results. This was probably because the interleaved task was similarly challenging for both hands, and required high dexterity. Therefore, differences in activity between the left and right hands were less apparent. Our results showed the modulation of activation intensity in the spinal cord by the dexterity.

Introduction

Contralateral activations found in the brain were revealed in 1973 by Brinkman and Kuypers (1973), who showed that right hand movements are associated with neural activity in the left motor cortex, while left hand movements are associated with neural activity in the right motor cortex. The action potential carrying the motor information travels along the white matter tract from the contralateral motor cortex of the cerebrum down to the midbrain, pons, and medulla oblongata, at which the neuronal fibers cross to the ipsilateral side and finally reach the spinal cord. Therefore, contralateral activations in the brain and ipsilateral activations in the spinal cord are both present.

The advances of magnetic resonance imaging (MRI) and positron emission tomography (PET) enable the investigation of tissue structure in vivo. Functional MRI (fMRI) and PET enable functional mapping of different activities in the central nervous system (CNS). Since the findings of Brinkman and Kuypers, (1973), researchers have been investigating the relationship between task complexity, dexterity, handedness, and functional activation of both ipsilateral and contralateral hemispheres (Jancke et al., 1998, Kawashima et al., 1993, Kim et al., 1993, Li et al., 1996, Rao et al., 1993, Singh et al., 1998, Wexler et al., 1997). It has been found that stronger brain functional activation is associated with left hand rather than right hand movement in right-handed individuals (Jancke et al., 1998, Kim et al., 1993). It has been suggested that right-handed individuals expend more effort performing with their non-preferred hand (Jancke et al., 1998), which means that the less skilled and competent system expends more effort (the anatomical studies of Amunts et al., 1996, cited in Jancke et al., 1998) and therefore provides more fMRI signals. The functional organization difference in the brain in response to task complexity has also been documented. It has been found that more functional areas are activated in the brain during complicated motor tasks than during simple tasks (Rao et al., 1993, Wexler et al., 1997). On the other hand, an ipsilateral activation component has been reported in brain fMRI studies with unilateral finger motion (Li et al., 1996, Singh et al., 1998). It shows that the activation induced in unilateral finger movement is not restricted to the contralateral cortex. This finding has also recently been confirmed in the cervical spinal cord using blood oxygenation level-dependent (BOLD) fMRI (Maieron et al., 2007). The recruitment of the ipsilateral cortex has also been shown to be more pronounced when participants use their non-dominant hand in fMRI (Singh et al., 1998) and PET (Kawashima et al., 1993) studies.

In the past 20 years, BOLD (Ogawa et al., 1990a, Ogawa et al., 1990b) and signal enhancement by extravascular protons (SEEP)-weighted (Stroman et al., 2002) fMRI have been introduced for imaging the human cervical spinal cord. The present study was focused on BOLD fMRI. Previous studies have shown that BOLD fMRI is feasible in the spinal cord at both 1.5 T and 3 T, and the activation areas detected have good localization at the segmental level (Govers et al., 2007, Madi et al., 2001, Maieron et al., 2007, Stroman et al., 1999, Stroman and Ryner, 2001, Yoshizawa et al., 1995). Although it has been shown that BOLD fMRI can be affected by the draining veins, especially at the surface of the spinal cord (Govers et al., 2007), modulation of activation can still be detected during upper limb movement (Madi et al., 2001, Maieron et al., 2007). It has been shown that there is a linear relationship between the applied force and the BOLD signal amplitude during isometric exercise (Madi et al., 2001), and that there is also a movement rate-dependent increase in spinal fMRI signals (Maieron et al., 2007). All these studies have shown that spinal BOLD fMRI is a reliable and sensitive tool for studying the modulation of functional activity in the spinal cord.

In the current study, we investigated the effect of dexterity on the BOLD activation intensity in the cervical spinal cord in right-handers. This was examined in the context of finger-tapping tasks in both sequential and interleaved order. Our hypothesis is that the modulation of the functional signal observed in the brain is also reflected in the spinal cord. Since the spinal cord is the output station of the CNS, by studying the modulation of the functional signal in the cervical spinal cord, functional activation for a specific task can be assessed directly.

Section snippets

Subjects

Ten right-handed healthy volunteers were recruited for this study. All were male, aged between 18 and 25 years, and had normal cervical spinal cords, without any history of disease or injury. The subjects included did not have any special training leading to different dexterity (none of the subjects knew how to play musical instruments and their typing speed was medium). Each subject gave fully informed consent prior to participating in the experiments. The protocol was approved by the Research

Results

For the difficulty measurement test, the time for doing 20 cycles of the interleaved tasks (LI and RI) was significantly longer than for the sequential tasks (LS and RS), using the Wilcoxon signed-rank test for paired samples (P < 0.001). This implies that tapping the fingers in interleaved order was more difficult than in sequential order.

For the fMRI studies, seven out of the 10 subjects recruited exhibited BOLD activation in all four fMRI sessions. When the translation and rotation parameters

Discussion

Our results showed that the functional activation induced in unilateral finger-tapping tasks could be detected inside the cervical spinal cord by using BOLD fMRI. Both ipsilateral and contralateral activations were detected in all seven subjects who had activation seen inside the spinal cord. This was consistent with our previous study (Ng et al., 2006) and the most recent studies (Maieron et al., 2007). It was found that the mean contrast value of the entire cervical spinal cord in the LS task

Conclusion

Our spinal BOLD fMRI results showed that the functional activation intensity in the sequential finger-tapping task using the non-dominant left hand was significantly higher than that for the dominant right hand in right-handed individuals. The increase in activation intensity arose from the fact that the non-dominant hand was less skilled and competent, and thus required additional processing power for doing the finger-tapping task, which produced a stronger fMRI signal. There were no

Acknowledgments

We would like to thank The Jockey Club Charity Trust and The Seed funding from The University of Hong Kong for their financial support. Disclosure: The authors have reported no conflicts of interest.

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