Movement-related neuromagnetic fields in preschool age children

Abstract

We examined sensorimotor brain activity associated with voluntary movements in preschool children using a customized pediatric magnetoencephalographic system. A videogame-like task was used to generate self-initiated right or left index finger movements in 17 healthy right-handed subjects (8 females, ages 3.2-4.8 years). We successfully identified spatiotemporal patterns of movement-related brain activity in 15/17 children using beamformer source analysis and surrogate MRI spatial normalization. Readiness fields in the contralateral sensorimotor cortex began ∼0.5 s prior to movement onset (motor field, MF), followed by transient movement-evoked fields (MEFs), similar to that observed during self-paced movements in adults, but slightly delayed and with inverted source polarities. We also observed modulation of mu (8-12 Hz) and beta (15-30 Hz) oscillations in sensorimotor cortex with movement, but with different timing and a stronger frequency band coupling compared to that observed in adults. Adult-like high-frequency (70-80 Hz) gamma bursts were detected at movement onset. All children showed activation of the right superior temporal gyrus that was independent of the side of movement, a response that has not been reported in adults. These results provide new insights into the development of movement-related brain function, for an age group in which no previous data exist. The results show that children under 5 years of age have markedly different patterns of movement-related brain activity in comparison to older children and adults, and indicate that significant maturational changes occur in the sensorimotor system between the preschool years and later childhood.

Keywords: MEG; beamformers; development; movement-related fields; mu rhythm; sensorimotor oscillations.

Figure 1

A: Photograph of 4.8‐year‐old girl positioned in the Yokagawa child MEG system holding the Lumitouch response pad while viewing the visual display located on the MSR ceiling. A screen image of the space‐game is shown below. B: Comparison of an averaged movement‐related field (filtered 1–15 Hz) timelocked to the button press for a sensor overlying the left sensorimotor cortex from an adult subject (recorded in a 160 channel MEG system) and a 4.4‐year‐old boy recorded in the 60‐channel child MEG system. Both systems were manufactured by KIT, Kanazawa, Japan and located side by side in the same magnetically shielded room. The field topographies of the MF and MEFI components are shown at the corresponding peak latency. Positive values indicate magnetic flux exiting the head (red colors) and negative flux entering the head (blue colors). Note the reversed field orientation and slight delayed latency of these components in the child. C: Examples of ERB analysis in two children for left hand versus right hand responses. The cartoon heads show the peak activity at the latency of the MF (t = 20 ms) and the corresponding time course filtered 0.3–30 Hz to show the slow readiness field beginning approximately 0.5 s prior to movement onset and transient MEFI component approximately 140 ms after movement onset. The latter is more distinct for the right (dominant) hand movements. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Source locations of the MF in individual subjects, shown in the MEG coordinate system for right button presses (top) and left button presses (bottom). Coordinate system corresponds to the CTF MEG coordinate system which is a right‐handed coordinate system with the +ve x‐axis toward the nose and +ve y‐axis toward the left ear. Locations for male subjects are shown as square symbols and for female subjects as circles. Note tighter clustering of sources for right compared to left button presses. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 3

A: Group averaged ERB source waveforms for all 15 subjects shown for right button press (blue trace) and left button press (red trace) conditions. Bandpass 0.3–30 Hz. Amplitude of the MF and MEFI components (asterisks) was significantly greater for right compared to left movements (asterisks). The peak locations of the MF for both movement conditions is shown superimposed on the MNI template brain, thresholded at the P < 0.01 level using surrogate MRI warping. Talairach coordinates for each peak are shown and correspond to locations near the hand area of the precentral gyrus. B: Time‐frequency plots of the group averaged induced power changes (averaged power subtracted) with increases (red) and decreases (blue) around movement onset (button press = 0 s) showing mu and beta band modulations and low and high gamma bursts at movement onset. Note delayed onset of mu and beta suppression and rebound, and absence of high gamma activity for left movements. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 4

A: Time–frequency plots of movement induced source activity in the gamma band (30–90 Hz) in contralateral motor cortex (MI) for left and right button presses in three different representative subjects that showed either only high frequency gamma activation around 80 Hz (first row), only low frequency gamma activation around 38 Hz (second row), or both high and low frequency gamma activation (third row) at movement onset (t = 0 s). B: Gamma band source activity in contralateral MI for both high gamma band (60–90 Hz) or low gamma range (30–60 Hz) averaged over all subjects. The black horizontal line and text (F _peak) shows the estimated peak frequency using bootstrap resampling of one‐half of all subjects. The length of the line shows the time period over which peak frequency was estimated (−0.3 to 0.3 s). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 5

Movement‐locked activation of a source in the right temporal gyrus was observed for both left and right button press conditions with peak activation at ∼70 ms. Source location shown in MNI coordinates, permutation threshold = P < 0.002. Note almost identical locations (shown in Talairach coordinates with corresponding atlas labels) for both conditions. These peaks showed remarkably similar time courses (shown below) peaking at latency of 70 ms (black arrow) with a slower activation around 0.5–0.7 s following movement onset. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]