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article info
Article history:
Accepted 8 March 2010
abstract
width partitioned for each rhythm reflects their underlying spec-
tral nature and that the peak frequency of mu and beta
responses typically differs between subjects. A large array of senso-
rimotor events have been shown to modulate these rhythms,
including tactile stimulation (Cheyne et al., 2003; Gaetz & Cheyne,
2006; Houdayer, Labyt, Cassim, Bourriez, & Derambure, 2006; Mul-
power several hundred milliseconds (up to 1500 ms) preceding
the movement onset that occurs in both beta and mu frequency
bands. Once the movement is terminated, a sharp increase in
power occurs for the beta-band within the next 1–2 s, whereas
power in the mu rhythm increases along a shallow slope lasting
several seconds (Pfurtscheller & Lopes da Silva, 1999; Pineda,
2005). The pre-movement decrease in power is typically termed
an event-related desynchronization or pre-movement ERD, and
the post-movement increase is an event-related synchronization
(ERS) or in this literature, the post-movement beta rebound
(PMBR). These oscillatory changes are normally gauged relative
* Corresponding author at: University of Nebraska Medical Center, 988422
Nebraska Medical Center, Omaha, NE 68198, USA. Fax: +1 402 559 5747.
E-mail addresses: Tony.W.Wilson@gmail.com, tonewilson@msn.com (T.W.
Brain and Cognition 73 (2010) 75–84
Contents lists availab
Brain and C
.eWilson).1. Introduction
Previous electrophysiological studies of motor function have
characterized the oscillatory dynamics of neural responses culmi-
nating in the sensorimotor cortices. Such oscillatory behavior be-
gins several hundred milliseconds preceding the movement onset
and continues for several seconds after movement termination.
These responses are commonly segregated into two quasi-distinct
frequency bands, a lower frequency mu rhythm (8–16 Hz) and a
higher frequency beta rhythm (15–30 Hz). The generous band-
ler et al., 2003; Neuper & Pfurtscheller, 2001), passive movements
(Cassim et al., 2001), voluntary movements (Cassim et al., 2001;
Houdayer et al., 2006; Jurkiewicz, Gaetz, Bostan, & Cheyne, 2006;
Parkes, Bastiaansen, & Norris, 2006; Pfurtscheller, Stancak, & Neu-
per, 1996; Salmelin, Hamalainen, Kajola, & Hari, 1995), imagined
movements (de Lange, Jensen, Bauer, & Toni, 2008; Pfurtscheller
& Neuper, 1997; Pfurtscheller, Neuper, Brunner, & Lopes da Silva,
2005), and even observing another agent’s movements (Hari
et al., 1998; Koelewijn, van Schie, Bekkering, Oostenveld, & Jensen,
2008). Generally, such modulation entails a sharp decrease inAvailable online 24 April 2010
Keywords:
Precentral
ERD
ERS
Synchronization
Cortex
MEG
Cerebellum
Magnetoencephalography
Somatosensory
Mu
Child0278-2626/$ - see front matter  2010 Elsevier Inc. A
doi:10.1016/j.bandc.2010.03.001This study examines the time course and neural generators of oscillatory beta and gamma motor
responses in typically-developing children. Participants completed a unilateral flexion–extension task
using each index finger as whole-head magnetoencephalography (MEG) data were acquired. These
MEG data were imaged in the frequency-domain using spatial filtering and the resulting event-related
synchronizations and desynchronizations (ERS/ERD) were subjected to voxel-wise statistical analyses
to illuminate time–frequency specific activation patterns. Consistent with adult data, these children
exhibited a pre-movement ERD that was strongest over the contralateral post-central gyrus, and a
post-movement ERS response with the most prominent peak being in the contralateral precentral gyrus
near premotor cortices. We also observed a high-frequency (80 Hz) ERS response that coincided with
movement onset and was centered on the contralateral precentral gyrus, slightly superior and posterior
to the beta ERS. In addition to pre- and post-central gyri activations, these children exhibited beta and
gamma activity in supplementary motor areas (SMA) before and during movement, and beta activation
in cerebellar cortices before and after movement. We believe the gamma synchronization may be an
excellent candidate signal of basic cortical motor control, as the spatiotemporal dynamics indicate the
primary motor cortex generates this response (and not the beta oscillations) which is closely yoked to
the initial muscle activation. Lastly, these data suggest several additional neural regions including the
SMA and cerebellum are involved in basic movements during development.
 2010 Elsevier Inc. All rights reserved.An extended motor network generates b
perturbations during development
Tony W. Wilson
a,b,
*
, Erin Slason
b
, Ryan Asherin
b
, E
Donald C. Rojas
b
a
Center for Magnetoencephalography, University of Nebraska Medical Center, Omaha, N
b
Neuromagnetic Imaging Center, Department of Psychiatry, University of Colorado, Den
journal homepage: wwwll rights reserved.a and gamma oscillatory
ne Kronberg
b
, Martin L. Reite
b
, Peter D. Teale
b
,
SA
School of Medicine, Denver, CO, USA
le at ScienceDirect
ognition
lsevier.com/locate/b&c

d Cto a baseline period that occurred 3–5 s from the most recent
movement (i.e., before and after movement). For excellent reviews,
see Hari and Salmelin (1997) or Pfurtscheller and Lopes da Silva
(1999).
These oscillatory perturbations are thought to reflect large-scale
changes in the synchronicity of sensorimotor networks. Essentially,
somatosensory and primary motor networks are thought to syn-
chronize at mu and beta frequencies, respectively, in the absence
of internal and/or external sensorimotor inputs. In the case of voli-
tional movements, the pre-movement ERD indicates a large-scale
desynchronization due to input disturbing the resting or idling fre-
quency of sensorimotor cortices. Although the ERD reflects a de-
crease in power, the underlying mechanism is believed to be
activation of a small patch(s) of cortex which serves the tactile per-
ception and/or motor output (Pfurtscheller & Lopes da Silva, 1999;
Pineda, 2005). Thus, pre-movement ERDs are large-scale decreases
in power that are putatively accompanied by a small-scale activa-
tion near the centroid or peak of the frequency-specific ERD. In
contrast, the PMBR may indicate the return of sensorimotor corti-
ces to their highly synchronous resting state following completion
of the sensory or motor task (i.e., the idling hypothesis; Pfurtschel-
ler, 1992; Pfurtscheller & Lopes da Silva, 1999; Pfurtscheller et al.,
1996); albeit, other models suggest the PMBR results from active
inhibition (Cassim et al., 2001; Pfurtscheller & Neuper, 1997; Sal-
melin et al., 1995) and/or somatosensory reafferent input to the
motor cortex (Cassim et al., 2001; Houdayer et al., 2006). Likewise,
the post-movement mu rebound may reflect an analogous phe-
nomena for this lower frequency band, but unlike the PMBR re-
sponse, mu rebound is slower, less intense, and does not exceed
the degree of baseline power in this brain area (i.e., before the
pre-movement ERD; Salmelin & Hari, 1994; Salmelin et al.,
1995). Studies of volitional movement in adults have shown mu
and beta responses localize to somatotopic areas of the post-cen-
tral and precentral gyrus, respectively (Pfurtschellar et al., 1994;
Pfurtscheller & Lopes da Silva, 1999; Salmelin & Hari, 1994; Salme-
lin et al., 1995). These studies did not note spatial differences be-
tween pre- and post-movement responses in either frequency
band. However, beta-band responses more closely followed soma-
totopic organization and showed more laterality than mu activity,
being stronger in the cortices contralateral to the movement. More
recent studies, especially those using magnetoencephalography
(MEG), have refined understanding of the pre- versus post-move-
ment responses in these bands. These studies have shown both
pre- and post-event (ERD and ERS) rhythmic mu activity localizes
to the post-central gyrus, shows moderate contralateral domi-
nance, and roughly follows the somatotopic organization of these
cortices (motor: Jurkiewicz et al., 2006; tactile stimulation: Cheyne
et al., 2003; Gaetz & Cheyne, 2006). In regards to the oscillatory
beta activity, these studies found pre-event beta ERD to be gener-
ated in the post-central gyrus and that the neural correlates of the
post-event beta ERS are slightly anterior in the precentral motor
cortex (Cheyne et al., 2003; Gaetz & Cheyne, 2006; Jurkiewicz
et al., 2006). Contralateral dominance and somato- or motorotopic
mapping was stronger for beta versus mu responses, especially for
the PMBR. However, a combined electroencephalography (EEG)
and functional magnetic resonance imaging (fMRI) study recently
reported a post-central gyrus focus for the PBMR motor response,
thus indicating that the source of this beta rebound remains some-
what uncertain (Parkes et al., 2006).
Although the regions generating PMBR activity remain an area
of contention, another facet of oscillatory motor behavior has only
recently seen widespread interest and thus, is far less character-
ized. Essentially, using invasive methods, a number of studies in
76 T.W. Wilson et al. / Brain anepilepsy patients have described high-frequency gamma responses
in the 65–100 Hz range during sustained muscle contractions, con-
tinuous movements, and a few other motor tasks (Brovelli, Lach-aux, Kahane, & Boussaoud, 2005; Miller et al., 2007; Pfurtscheller,
Graimann, Huggins, Levine, & Schuh, 2003; Szurhaj et al., 2006).
The brain areas generating this activity are near precentral gyrus
and other motor areas, but their precise location has been limited
to the region where the grid or subdural electrode was placed dur-
ing surgery. Likewise, the motor tasks used in these studies have
limited extraction of time course information. However, a few re-
cent MEG studies have described similar gamma activity in sensors
near motor cortex (Schoffelen, Oostenveld, & Fries, 2005; Waldert
et al., 2008), or precisely in the hand region of primary motor cor-
tex (Cheyne, Bells, Ferrari, Gaetz, & Bostan, 2008; Tecchio et al.,
2008). Cheyne et al. (2008) demonstrated that high-frequency
gamma responses coincided with the movement onset, were
strongly lateralized to the contralateral hemisphere, and largely
followed the somatotopic organization of the primary motor cortex
with respect to the foot, bicep and index finger. These findings
have not yet been replicated, but their spatiotemporal dynamics
are intriguing as the response could reflect the initial activation
of primary motor neurons serving movement, or a form of feed-
back allowing advanced control of discrete movements (see Chey-
ne et al., 2008). As noted above, a previous study by this same
group found PMBR activity also localized to the contralateral pri-
mary motor area. Indeed, for the same right index finger move-
ment, the PMBR activation peak in the earlier study (Jurkiewicz
et al., 2006) was within 1 mm on x- and y-axis and only 5 mm
superior (z-axis) to the peak for high-gamma activity (Cheyne
et al., 2008). This could indicate a common population of neurons
generates the two responses at different stages of movement exe-
cution, with the time course and spectral content simply reflecting
the diverse functions necessary for these distinct phases of move-
ment. Although it is worth noting that the spatial similarity be-
tween PMBR and high-frequency gamma could be artificial, as to
date the two responses have not been characterized in the same
group of participants. Thus, even in healthy adults, the precise
neural generators of gamma- and beta-frequency oscillatory motor
responses, there spatiotemporal relationships, and their neurobe-
havioral functions remain a work in progress. In regards to distin-
guishing function within the motor system, a substantial body of
fMRI data is now available although it is difficult to directly link
with neural oscillatory activity. The primary motor cortices appear
to be the most basic element and are involved in the initiation of
movement amongst many other functions (Passingham, 1997;
Ween, 2008). Several studies have shown the supplementary mo-
tor cortex is intricately involved in coordinating bimanual move-
ments (Koeneke, Lutz, Wustenberg, & Jancke, 2004; Swinnen,
2002) and unimanual movements that involve sequencing or
maintaining an internal pace (Jenkins, Jahanshahi, Jueptner, Pass-
ingham, & Brooks, 2000; Passingham, Chen, & Thaler, 1989). There
is also strong evidence that multiple regions of the premotor cortex
and the cerebellum are involved in bimanual tasks, and that these
regions become more strongly recruited as the task complexity in-
creases (Debaere, Wenderoth, Sunaert, Van Hecke, & Swinnen,
2004). Several excellent reviews of different components of the
motor system are available (Geyer, Matelli, Luppino, & Zilles,
2000; Nachev, Kennard, & Husain, 2008; Passingham, 1997; Rizzol-
atti & Luppino, 2001).
In this study, we examine the oscillatory dynamics of basic mo-
tor circuitry by recording high-density MEG data during unilateral
flexion–extension movements of each index finger in a group of
typically-developing children and adolescents. Previous MEG and
EEG investigations of oscillatory motor activity have focused exclu-
sively on adults and have not studied the full gamut of responses.
Thus, the aims of the current study were to derive the spatial and
ognition 73 (2010) 75–84temporal relationship of the full range of oscillatory responses in a
single group of participants, and to assess the effect of maturation
on oscillatory motor activity. Our primary hypothesis was that