Post-movement beta rebound is generated in motor cortex: Evidence from neuromagnetic recordings
Introduction
Neural activity within primary sensorimotor cortex of the human brain has long been known to exhibit oscillatory behavior. Of particular interest have been oscillations within two specific frequency bands, the beta (15–30 Hz) and mu (8–14 Hz) bands, as they have been shown to be modulated during and following the preparation and performance of voluntary movement (Salmelin et al., 1995, Pfurtscheller et al., 1996, Leocani et al., 1997, Cassim et al., 2001, Parkes et al., 2006), passive movement (Cassim et al., 2001), imagined movement (Pfurtscheller et al., 2005), and even tactile stimulation (Neuper and Pfurtscheller, 2001, Cheyne et al., 2003, Gaetz and Cheyne, 2006). These oscillations have been suggested to reflect an idling cortex generated by a large area of highly synchronous neuronal firing in the absence of input, or alternatively, changes in coherent activity resulting from synchronous input from other brain regions.
Modulation of the beta and mu band oscillations that accompany voluntary movement has been described and takes one of two forms. Beginning as early as 2 s prior to movement initiation (Pfurtscheller and Berghold, 1989, Leocani et al., 1997), a reduction in oscillatory power in both the beta and mu frequency bands, known as event-related desynchronization (ERD), has been observed to originate over contralateral sensorimotor areas (see Pfurtscheller and Lopes da Silva, 1999 for review). Desynchronization of these oscillations, the result of asynchronous activity within these cortical networks, is thought to be related to neural activation (Pfurtscheller and Berghold, 1989). Following movement termination, while mu power returns slowly to baseline (Salmelin and Hari, 1994, Salmelin et al., 1995, Leocani et al., 1997), beta power consistently returns to and exceeds pre-movement levels (Pfurtscheller et al., 1996). This event known as event-related synchronization (ERS) begins within several hundred milliseconds of movement termination and persists for several hundred more. Although it is generally believed that ERS reflects a neural deactivation, the so-called ‘idling’ hypothesis (Pfurtscheller et al., 1996, Cassim et al., 2001), this specific beta band ERS that follows movement termination is known as post-movement beta rebound (PMBR) and has been suggested to represent an inhibition of motor cortex (Salmelin et al., 1995) or a sensory reafference (Cassim et al., 2001). Although the underlying neurophysiological mechanisms producing movement-related cortical oscillations, and their functional significance for motor control are not fully understood, the precise location of the neural sources for specific rhythmic activity is beginning to be identified through the use of electrophysiological techniques with high temporal and spatial resolution.
Electroencephalography (EEG) studies have identified both beta and mu ERD during finger movement to be maximal over contralateral sensorimotor cortex, with a similar contralateral sensorimotor cortical location for maximal beta ERS following movement termination (Pfurtscheller et al., 1996, Leocani et al., 1997, Cassim et al., 2001). Further study has revealed that the location of beta band ERS is slightly more anterior to the mu ERD, suggesting that at least some components of the beta rhythm are generated in the pre-Rolandic motor area while the mu rhythm is generated mainly in the post-Rolandic somatosensory area (Pfurtscheller et al., 1996). A similar study employing magnetoencephalography (MEG) also identified a clear difference between the spatial and temporal occurrence of the beta and mu rhythms, with beta frequency oscillations generated predominantly in the anterior bank of the central sulcus, while the generator of mu frequency oscillations extended well into the postcentral cortex (Salmelin et al., 1995). A recent study combining functional magnetic resonance imaging (fMRI) and EEG (Parkes et al., 2006), however, suggests that the region of blood oxygen level-dependent (BOLD) signal increase most significantly related to PMBR is located posterior to the central sulcus. They concluded that the source of this rebound is in the parietal cortex and thus may be more related to sensory afference than to inhibition of the motor cortex. These new findings cast some doubt on the precise location of the source of beta band ERS following movement termination and thus, the potential role of this post-movement rebound.
Although EEG has been used extensively for the investigation of cortical oscillatory behavior, MEG provides a great advantage in that source localization is less affected by the varying conductivity of the overlying tissues and can therefore be more accurately modeled than with EEG. With a temporal resolution on the order of milliseconds, MEG also provides the ability to differentiate neural activity on a time scale not possible with fMRI. In addition, new spatial filtering approaches to the analysis of MEG data, such as the synthetic aperture magnetometry (SAM) method, have been shown to be able to successfully detect time-locked increases (ERS) and decreases (ERD) in the beta and mu frequency bands in the vicinity of the central sulcus during median nerve stimulation (Cheyne et al., 2003, Hirata et al., 2002, Gaetz and Cheyne, 2003), and voluntary hand movements (Taniguchi et al., 2000, Cheyne et al., 2006). Neuromagnetic source localization therefore provides the best opportunity to identify precise spatial and temporal changes in frequency-specific sensorimotor cortical oscillations. The objective of this study was to identify the time course of oscillatory activity in the beta and mu frequency bands associated with voluntary finger movement and the source of these rhythms using spatially filtered neuromagnetic imaging; an approach not yet applied to the investigation of these oscillations during to the preparation and execution of voluntary movement.
Section snippets
Subjects
Ten subjects (five male; mean age 32.3 years, range = 21–47) participated in the experiment after providing informed consent using protocols approved by The Hospital for Sick Children Research Ethics Board. All subjects were considered healthy without prior history of neurological illness and right hand dominant. Subjects were asked to lay on a comfortable bed with their eyes open in a magnetically shielded room. Each subject was fitted with three fiducial localization coils placed at the nasion
Time course of oscillatory changes accompanying movement
To identify the time course of oscillatory changes within sensorimotor cortex associated with voluntary movement, time-frequency analysis was performed on the SAM virtual sensors computed at the location of maximal beta ERS in both the contralateral and ipsilateral hemispheres. Time-frequency (TFR) plots of these virtual sensors (Fig. 1A) demonstrate clear patterns of suppression (ERD) and enhancement (ERS) of oscillatory activity in the beta and mu frequency bands prior to, during, and
Discussion
This study describes the time course of change in oscillatory activity in the beta and mu frequency bands that accompany voluntary movement, and identifies the location of the neural sources involved in the generation of these rhythms. During execution of a voluntary movement, a strong suppression, ERD, in both beta and mu band power was detected bilaterally over the hand region of sensorimotor cortex; ERD in both frequency bands was greater contralateral to the side of movement. Mu band ERD
Acknowledgments
This research was supported by the Canadian Institutes for Health Research (Grant 64279) and the Natural Sciences and Engineering Research Council of Canada (Grant 104018-04).
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