Changes in brain activation patterns according to cross-training effect in serial reaction time task: An functional MRI study

Abstract

Cross-training is a phenomenon related to motor learning, where motor performance of the untrained limb shows improvement in strength and skill execution following unilateral training of the homologous contralateral limb. We used functional MRI to investigate whether motor performance of the untrained limb could be improved using a serial reaction time task according to motor sequential learning of the trained limb, and whether these skill acquisitions led to changes in brain activation patterns. We recruited 20 right-handed healthy subjects, who were randomly allocated into training and control groups. The training group was trained in performance of a serial reaction time task using their non-dominant left hand, 40 minutes per day, for 10 days, over a period of 2 weeks. The control group did not receive training. Measurements of response time and percentile of response accuracy were performed twice during pre- and post-training, while brain functional MRI was scanned during performance of the serial reaction time task using the untrained right hand. In the training group, prominent changes in response time and percentile of response accuracy were observed in both the untrained right hand and the trained left hand between pre- and post-training. The control group showed no significant changes in the untrained hand between pre- and post-training. In the training group, the activated volume of the cortical areas related to motor function (i.e., primary motor cortex, premotor area, posterior parietal cortex) showed a gradual decrease, and enhanced cerebellar activation of the vermis and the newly activated ipsilateral dentate nucleus were observed during performance of the serial reaction time task using the untrained right hand, accompanied by the cross-motor learning effect. However, no significant changes were observed in the control group. Our findings indicate that motor skills learned over the 2-week training using the trained limb were transferred to the opposite homologous limb, and motor skill acquisition of the untrained limb led to changes in brain activation patterns in the cerebral cortex and cerebellum.

Keywords: cerebellar activation; cortical activation; cross-training effects; dentate nucleus; functional MRI; grants-supported paper; motor skill learning; neural regeneration; neuroimaging; neuroregeneration; photographs-containing paper; primary motor cortex; response accuracy; response time; serial reaction time task; vermis.

Figure 1

Pre- and post-training changes in cerebral cortex activation during sequential finger movement using the right untrained hand in the training and control groups. (A) Sequential finger movement induced cortical activation on the bilateral primary sensorimotor cortex, bilateral premotor cortex, and bilateral posterior parietal cortex in the first functional MRI scans in the training and control groups. Following 2 weeks of training with the left hand, activation on the ipsilateral premotor cortex and posterior parietal cortex decreased, and contralateral activation on the primary sensorimotor area, premotor cortex, and posterior parietal cortex decreased, in the training and control groups. However, the left primary sensory motor area activity was significantly decreased in the training group compared with the control group. (B) In the first functional MRI scans for the cerebellar regions, the ipsilateral cerebellar areas (left dentate nucleus) showed activation during rapid sequential finger movement in the training and control groups, and greater activation of the medial cerebellar area (vermis) in the training group. After 2 weeks of training with the left hand, an obvious increase in neural activation was observed in the vermis and the left dentate nucleus. In the control group, cortical activation of the left dentate nucleus was slightly increased and the vermis was newly activated. In the highlighted bar for the activated peak voxel, the yellow color indicates higher neural activation than the red color.

Figure 2

Schematic of the experiment. (A) Example of training setting. Subjects were instructed to repeatedly push the four numbered response buttons as accurately and quickly as possible using the non-dominant (left) hand during the task block. (B) Composition of the training paradigms. One training session was composed of display for 10 seconds, training for 4 minutes 50 seconds, and rest for 3 minutes, repeated five times. (C) Timetable of motor training and functional MRI (fMRI) experiments in the training group.