Automatic activation in the human primary motor cortex synchronized with movement preparation

Abstract

The human primary motor cortex during a unilateral finger reactive movement to visual stimuli was examined by magnetoencephalography (MEG) measurement. The brain activity related to movement execution (the motor activity contralateral to the movement side) was estimated based on movement onset conditions and reaction times. The movement onset conditions were: (1) a simple reaction time task with a visual stimulus, (2) a Go/NoGo task with different colored stimuli and (3) a Go/NoGo task with different position stimuli. Dipole source estimation was done, and the time course of the motor activity was calculated. The results showed that not only the visual response but also the contralateral motor activity was evoked by the stimulus in all cases, and even when the NoGo stimulus was given. The motor activity in the primary motor cortex was conjectured to consist of two dominant components: the first component for the movement preparation and the second component for the movement execution. Because the first component happened with a constant delay time from the stimulus even in the NoGo case, the first component, coming through a fast pathway for signals from visual stimulus processing to the motor cortex without any intervening cognitive processing, was conjectured to make the motor cortex prepare for the forthcoming movement onset automatically regardless of the stimulus instruction.

Introduction

It has been known, through both invasive and non-invasive measurements, that a variety of brain motor areas, including the supplementary motor area (SMA), pre-motor area and primary motor area, are active during a movement and that the sensory area is also activated by the movement. Invasive recordings in primates, which measure specific neuron discharges, have examined the neuron activity associated with the movements, the projections between each area, and their functional role 2, 33. In humans, attempts to clarify the role of each area have been made by recordings with chronically implanted subdural electrodes 19, 20, 26. These invasive recordings have shown the effectiveness of measuring the brain activity and the functional anatomy directly, but there are restrictions in the experimental procedure. In contrast, PET and fMRI are useful non-invasive methods where most activity related to regional cerebral blood flow can be identified 3, 4, 11, 25, 32. However these methods measure signals caused by changes in blood flow and have limitations of temporal resolution. EEG recording is also a useful non-invasive method that reveals the time course of activities through overlapped potentials 10, 16, 37, 41and recently has been analyzed by dipole source modeling 5, 31, 42. However, the data of these potentials most likely contain the activities of several areas, and it has been difficult to discriminate precisely the location and contribution of each activity. Consequently, these non-invasive measurements have serious limitations of spatial or temporal resolution.

Magnetoencephalography (MEG) measurement is another useful non-invasive measurement method that has made it possible to map activity sources at their peak latencies with high spatio-temporal resolution and which has been used in human brain research. Because MEG measurement has high sensitivity only for the tangential components of neuron activities in the brain [35], the sources in the primary sensorimotor cortex have been investigated for movement-related activity 6, 7, 8, 12, 18, 21, 24, 28. In a self-paced brisk movement, a slow magnetic field shift called the readiness field (RF) starts 500–1000 ms prior to the movement onset, and it shows a slight increase in amplitude around EMG onset (the motor field (MF)). RF and MF have been interpreted as the activity generated from the primary motor cortex (MI), since SMA is not detectable in normal subjects [24]and the premotor area (PMA) has been said to be difficult to measure because of its radial orientation [21]. After EMG onset, a peak in the movement-evoked field is observed at 100 ms (MEFI) and at 200 ms (MEFII) 6, 12, 18, 21. MEFI is the most prominent activity that has been identified as activity in the primary sensor cortex (SI). MEFI is known to be a reafferent input to the contralateral sensory area from the moving muscles, e.g., from the deep receptors of muscle spindles 9, 21.

However, despite the many MEG studies related to movement execution, not much is known about temporal features in the human sensorimotor cortex. Although a few studies to extrapolate the time course of activity have been done in self-paced movements (SPM) 7, 8, 13, 18, few estimations of activity have been done for a signal-triggered movement 14, 28. Only one report of a simple reaction time (RT) task with an LED visual stimulus has shown that motor activity synchronized with the stimulus onset was observed [14]. The purpose of the present investigation is to elucidate the temporal features of the activities in the primary motor cortex. This study focuses on the brain activity related to the movement execution (the motor activity contralateral to the movement side) and reports how the time course of this motor activity changes depending on the movement onset conditions. In this study, a visual stimulus was used as an external instruction to elicit the motor activity synchronized not only with the movement onset (EMG onset) but also with the movement initiation (stimulus onset). In order to examine whether the motor activity depends on the movement condition or not, a comparison between the self-paced and stimulus triggered movement, and an analysis based on the RT were done.