Elsevier

NeuroImage

Volume 32, Issue 4, 1 October 2006, Pages 1709-1721
NeuroImage

Lateralization of brain activity during lower limb joints movement. An fMRI study

https://doi.org/10.1016/j.neuroimage.2006.05.043Get rights and content

Abstract

Studies of unilateral finger movement in right-handed subjects have shown asymmetrical patterns of activation in primary motor cortex and subcortical regions. In order to investigate the existence of an analogous pattern during lower limb joints movements, functional magnetic resonance imaging (fMRI) was used. Eighteen healthy, right leg dominant volunteers participated in a motor block design study, performing unilateral right and left repetitive knee, ankle and toes flexion/extension movements. Aiming to relate lower limb joints activation to the well-described patterns of finger movement, serial finger-to-thumb opposition was also assessed. All movements were auditory paced at 72 beats/min (1.2 Hz). Brain activation during movement of the nondominant joints was more bilateral than during the same movement performed with the dominant joints. Finger movement had a stronger lateralized pattern of activation in comparison with lower limb joints, implying a different functional specialization. Differences were also evident between the joints of the lower limb. Ankle and toes movements elicited the same extend of MR signal change in the majority of the examined brain regions, whereas knee joint movement was associated with a different pattern. Finally, lateralization index in primary sensorimotor cortex and basal ganglia was significantly affected by the main effect of dominance, whereas the lateralization index in cerebellum was significantly affected by the joint main effect, demonstrating a lateralization index increase from proximal to distal joints.

Introduction

Brain asymmetry has been observed in animals and humans in terms of structure, function and behavior. This lateralization of brain activity is thought to reflect evolutionary, hereditary, developmental, experiential and pathological conditions. Gender, limb dominance, motor skill specialization and trauma are a few selected factors that may influence the lateralization of brain activity (Toga and Thompson, 2003).

Lateralization of primary sensorimotor cortex activity during upper limb movements and the influence of dominance have received a lot of research attention. There is evidence that bilateral activation is more pronounced during the nondominant than the dominant unilateral hand movement, especially in right-handed subjects (Kim et al., 1993, Singh et al., 1998b, Volkmann et al., 1998). In left-handed subjects, there is a less lateralized pattern during both dominant and nondominant hand movements (Kim et al., 1993, Singh et al., 1998b). A few recent papers have suggested that there is a decrease of signal change in the ipsilateral SM1 during the movement of the dominant hand, although both the underlying mechanisms and the neurophysiological significance of this phenomenon remain unclear (Allison et al., 2000, Hamzei et al., 2002, Nirkko et al., 2001, Reddy et al., 2000). Lastly, there is an indication that in proximal tasks, such as shoulder movement, SM1 is bilaterally activated, although in distal tasks, such as finger movement, ipsilateral SM1 is less activated during the movement of the dominant limb (Nirkko et al., 2001).

In contrast to the primary sensorimotor cortex asymmetrical activation found during upper limb tasks, few reports exist regarding the subcortical regions. Scholz et al. (2000) found a left predominance pattern of basal ganglia activity during finger tapping in right handers, regardless of the hand used, assuming that the motor activation asymmetry found in that subcortical structure was even stronger than that in the primary motor cortex. Furthermore, a left predominance of SMA-proper has been detected during the movement of both dominant and nondominant hand (Babiloni et al., 2003, Rogers et al., 2004). It could be concluded that certain subcortical areas present asymmetric activation patterns as a result of the increased necessity of inhibitory pathways in order to reinforce upper limb dominance and play a prevailing role in the control of voluntary movements.

There is diminished evidence concerning the activation pattern of the lower limb joints movement. Despite the fact that a few studies have dealt with the lower limb joints in humans (Chainay et al., 2004, Debaere et al., 2001, Dobkin et al., 2004, Endo et al., 2004, Grodd et al., 2001, Lafleur et al., 2002, Luft et al., 2002, MacIntosh et al., 2004, Rotte et al., 2002), the pattern of brain activity in cortical and subcortical regions during motion of isolated lower limb joints and the influence of dominance on laterality of brain activity remain undetermined issues. Therefore, the purposes of this study were (1) to examine the pattern of brain activity in cortical and subcortical regions during the motion of unilateral isolated joints of lower limb in right-footed subjects, (2) to relate this pattern of brain activity during lower limb movements to the analogues activity during the finger tapping and (3) to study the influence of limb dominance and joint specificity (proximal or distal) on the lateralization of selected brain regions activity.

Section snippets

Subjects

Eighteen right leg dominant volunteers (males, aged 27 ± 5 years; range 22–35 years) with no special sport or habitual physical activity participated in this study, after giving written informed consent in accordance with Helsinki Declaration. The Baecke Questionnaire was used to assess their activity level (Baecke et al., 1982, Pereira et al., 1997). All subjects underwent a comprehensive verbal screen to ensure that they did not meet any of the exclusive criteria for fMRI experimentation: (1)

Subjects

Table 1 presents the demographic characteristics and performance scores of the subjects (n = 18). Subjects were right footed (mean WFQM and WFQS score of the subjects was 7.4 ± 2.2 and 6.0 ± 2.5 respectively). The functional hop tests showed a 2.2 to 4.0% increased functional ability of the right leg compared to the left one. Furthermore, the group was homogeneous with regard to the demographic characteristics and the activity level (Baecke questionnaire score 8.2 ± 1.1).

Network of activation

Isolated lower limb

Subjects

The objective of the present study was to examine brain asymmetric activity during lower limb movements and upper limb (finger) movements and describe the effects of dominance and joint specificity. However, the lateralization of brain activity can be influenced by several factors such as gender, motor skill specialization and trauma (Toga and Thompson, 2003). A number of studies have pointed to differences in brain asymmetry between males and females, some indicating that the male brain might

Conclusions

This paper emerges differences in brain activation during finger and lower limb joints movements with regard to the MR signal change and lateralization index. The more bilateral brain activation during lower limb joints compared to finger movement and the different extent to which several cortical and subcortical regions were involved (finger movement resulted in a higher degree of involvement of contralateral primary sensorimotor cortex and ipsilateral cerebellum whereas all joints of lower

Acknowledgments

We are grateful to Dr. P. Mparas, Dr. G. Seimenis (Philips) and Dr. A. Mantas for their technical support. We appreciate the help of Mr. S. Vasileiadis and Ms F. Valanou for their technical help in performing the scan sessions. We wish to thank Mr. V. Ladopoulos for the casts’ design and construction, Dr. M. Callaghan and Mr. M. Papadopoulos for their help in obtaining EMG data and Dr. Michalis Papathomas for his advice on statistics. We also acknowledge all volunteers that have participated in

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