Long-term motor training induced changes in regional cerebral blood flow in both task and resting states

Abstract

Neuroimaging studies of functional activation often only reflect differentiated involvement of brain regions compared between task performance and control states. Signals common for both states are typically not revealed. Previous motor learning studies have shown that extensive motor skill training can induce profound changes in regional activity in both task and control states. To address the issue of brain activity changes in the resting-state, we explored long-term motor training induced neuronal and physiological changes in normal human subjects using functional magnetic resonance imaging (fMRI) and positron emission tomography (PET). Ten healthy subjects performed a finger movement task daily for four weeks, during which three sessions of fMRI images and two sessions of PET images were acquired. Using a classical data analysis strategy, we found that the brain activation increased first and then returned to the pre-training, replicating previous findings. Interestingly, we also observed that motor skill training induced significant increases in regional cerebral blood flow (rCBF) in both task and resting states as the practice progressed. The apparent decrease in activation may actually result from a greater increase in activity in the resting state, rather than a decrease in the task state. By showing that training can affect the resting state, our findings have profound implications for the interpretation of functional activations in neuroimaging studies. Combining changes in resting state with activation data should greatly enhance our understanding of the mechanisms of motor-skill learning.

Fig. 1

Learning curves for the trained sequence. Each curve depicts the performance (movement speed: sequences per-minute) of a single subject or the statistical performance (mean and standard derivation as denoted by the error bar) as a function of time.

Fig. 2

Averaged (across subjects) fMRI activation maps (threshold: Z=2.5). Data were acquired on (A) pre-practice, (B) Week 2, and (C) Week4. The slices are 44, 38, 32, 26, 20, −36 mm from the AC-PC line, respectively. The letter L indicates the left side of the brain.

Fig. 3

Changes in activation volumes as training progressed. The activation volumes in M1 and SMA first increased and then returned to the pre-training state. The error bars represent one SEM (standard error of measurement).

Fig. 4

Averaged (across subjects) PET activation maps of motor skill training (threshold: Z=2.5). Data were acquired on (A) pre-training and (B) Week4. The slices are 44, 38, 32, 26, 20, −36 mm from the AC-PC line, respectively. The letter L indicates the left side of the brain.

Fig. 5

Mean voxel values of seven VOIs detected by PET. Regional blood flows in both task and resting state were measured at pre- and post-training. Motor skill training induced significantly increases in regional blood flow in both task and resting state (p <0.05). rM1: the right primary motor area, lM1: the left primary motor area, rPMd: the right dorsal premotor cortex, lPMd: the left dorsal premotor cortex, rCB: the right cerebellum, lCB: the left cerebellum, and SMA: supplementary motor area. The error bars represent one SEM.

Fig. 6

Power spectral analysis of resting state fMRI data. (A) The right M1 area; (B) the left M1 area. The right M1 area shows a significant increase in spectral power in the 0.08 Hz frequency band (p = 0.05). The left M1 area shows no significant increase in spectral power. The 0.08 Hz frequency band corresponds to the BOLD fluctuation frequency induced by spontaneous firing of neurons. The curves show differences between spectra obtained on Week 4 and pre-practice (Week 0) and on Week 2 and pre-practice (Week 0).