Douglas Cheyne

This work is the first evidence for frequency detuning of an intrinsic motor rhythm in spatially contiguous regions of primary motor cortex associated with hand and speech movements, supporting a mechanism of functional segregation that has been largely overlooked by current models of motor cortex organization. Our results from children further provide the first evidence for frequency detuning in the developing brain, indicating an early-developing mechanism with later refinements of hemispheric control.

Dystonia is a movement disorder characterized by repetitive muscle contractions, twisting movements, and abnormal posture, affecting 20% of pediatric arterial ischemic stroke (AIS) survivors. Recent studies have reported that children with dystonia are at higher risk of cognitive deficits. The connection between impaired motor outcomes and cognitive impairment in dystonia is not fully understood; dystonia might affect motor control alone, or it could also contribute to cognitive impairment through disruptions in higher‐order motor processes. To assess the functional correlates underlying motor control in children with dystonia, we used magnetoencephalography (MEG) to measure frontal theta (4–8 Hz), motor beta (15–30 Hz), and sensorimotor gamma (60–90 Hz) activity during a “go”/“no‐go” task. Beamformer‐based source analysis was carried out on 19 post‐stroke patients: nine with dystonia (mean age = 13.78, SD = 2.82, 8 females), 10 without dystonia (mean age = 12.90, SD = 3.54, 4 females), and 17 healthy controls (mean age = 12.82, SD = 2.72, 8 females). To evaluate inhibitory control, frontal theta activity was analyzed during correct “no‐go” (successful withhold) trials. To assess motor execution and sensorimotor integration, movement time‐locked beta and sensorimotor gamma activity were analyzed during correct “go” trials. Additionally, the Delis‐Kaplan Executive Function System (DKEFS) color‐word interference task was used as a non‐motor, inhibitory control task to evaluate general cognitive inhibition abilities. During affected hand use, dystonia patients had higher “no‐go” error rates (failed withhold) compared to all other groups. Dystonia patients also exhibited higher frontal theta power during correct withhold responses for both affected and unaffected hands compared to healthy controls. Furthermore, dystonia patients exhibited decreased movement‐evoked gamma power and gamma peak frequency compared to non‐dystonia patients and healthy controls. Movement‐related beta desynchronization (ERD) activity was increased in non‐dystonia patients for both hands compared to healthy participants. These results confirm that post‐stroke dystonia is associated with impaired frontally mediated inhibitory control, as reflected by increased frontal theta power. Post‐stroke dystonia patients also exhibited reduced motor gamma activity during movement, reflecting altered sensorimotor integration. The increased beta ERD activity in non‐dystonia patients may suggest compensatory sensorimotor plasticity not observed in dystonia patients. These findings suggest that differences in motor outcomes in childhood stroke result from a combination of cognitive and motor deficits.

Childhood apraxia of speech (CAS) is conceived as an impairment of the central motor system's ability to program multiple speech movements, resulting in inaccurate transitions between and relative timing across speech sounds. However, the extant neuroimaging evidence base is scant and inconclusive, and the neurophysiological origins of these motor planning problems remain highly underspecified. In the first magnetoencephalography study of this disorder, we measured brain activity from typically developing (TD) children (N = 19, 11 males, 8 females) and children with CAS (N = 7 males) during performance of a speech task designed to interrogate function of the speech areas of the primary sensorimotor cortex. Relative to their TD peers, our sample of children with CAS showed abnormal speech-related responses within the mu-band motor rhythm, and beamformer source reconstruction analyses specify a brain origin of this speech rhythm in the left cerebral hemisphere, within or near pre-Rolandic motor areas crucial for the planning and control of speech and oromotor movements. These results provide a new and specific candidate mechanism for the core praxic features of CAS; point to a novel and robust neurophysiological marker of typical and atypical expressive speech development; and support an emerging neuroscientific consensus which assigns a central role for programming and coordination of speech movements to the motor cortices of the precentral gyrus.

The brain must generate different motor signals depending on which hand is used. The distribution and timing of hand use/instructed motor plan integration are not understood at the whole brain level. Using MEG we show that different action planning subnetworks code for hand usage and integrating hand use into a hand-specific motor plan. The timing indicates that frontal cortex first creates a general motor plan and then integrates hand specificity to produce a hand-specific motor plan.

Cognitive control of action is associated with conscious effort and is hypothesised to be reflected by increased frontal theta activity. However, the functional role of these increases in theta power, and how they contribute to cognitive control remains unknown. We conducted an MEG study to test the hypothesis that frontal theta oscillations interact with sensorimotor signals in order to produce controlled behaviour, and that the strength of these interactions will vary with the amount of control required. We measured neuromagnetic activity in 16 healthy adults performing a response inhibition (Go/Switch) task, known from previous work to modulate cognitive control requirements using hidden patterns of Go and Switch cues. Learning was confirmed by reduced reaction times (RT) to patterned compared to random Switch cues. Concurrent measures of pupil diameter revealed changes in subjective cognitive effort with stimulus probability, even in the absence of measurable behavioural differences, revealing instances of covert variations in cognitive effort. Significant theta oscillations were found in five frontal brain regions, with theta power in the right middle frontal and right premotor cortices parametrically increasing with cognitive effort. Similar increases in oscillatory power were also observed in motor cortical gamma, suggesting an interaction. Right middle frontal and right precentral theta activity predicted changes in pupil diameter across all experimental conditions, demonstrating a close relationship between frontal theta increases and cognitive control. Although no theta-gamma cross-frequency coupling was found, long-range theta phase coherence among the five significant sources between bilateral middle frontal, right inferior frontal, and bilateral premotor areas was found, thus providing a mechanism for the relay of cognitive control between frontal and motor areas via theta signalling. Furthermore, this provides the first evidence for the sensitivity of frontal theta oscillations to implicit motor learning and its effects on cognitive load. More generally these results present a possible a mechanism for this frontal theta network to coordinate response preparation, inhibition and execution.

Articulography and functional neuroimaging are two major tools for studying the neurobiology of speech production. Until now, however, it has generally not been possible to use both in the same experimental setup because of technical incompatibilities between the two methodologies. Here we describe results from a novel articulography system dubbed Magneto-articulography for the Assessment of Speech Kinematics (MASK), used for the first time to obtain kinematic profiles of oro-facial movements during speech together with concurrent magnetoencephalographic (MEG) measurements of neuromotor brain activity. MASK was used to characterise speech kinematics in a healthy adult, and the results were compared to measurements from the same participant with a conventional electromagnetic articulography (EMA) setup. We also characterised speech movement kinematics with MASK in a group of ten typically developing children, aged 8-12 years. Analyses targeted the gestural landmarks of the utterances /ida/, /ila/ and reiterated productions of /pataka/. These results demonstrate that the MASK technique can be used to reliably characterise movement profiles and kinematic parameters that reflect development of speech motor control, together with MEG measurements of brain responses from speech sensorimotor cortex. This new capability sets the stage for cross-disciplinary efforts to understand the developmental neurobiology of human speech production.

Our ability to control and inhibit automatic behaviors is crucial for negotiating complex environments, all of which require rapid communication between sensory, motor, and cognitive networks. Here, we measured neuromagnetic brain activity to investigate the neural timing of cortical areas needed for inhibitory control, while 14 healthy young adults performed an interleaved prosaccade (look at a peripheral visual stimulus) and antisaccade (look away from stimulus) task. Analysis of how neural activity relates to saccade reaction time (SRT) and occurrence of direction errors (look at stimulus on antisaccade trials) provides insight into inhibitory control. Neuromagnetic source activity was used to extract stimulus‐aligned and saccade‐aligned activity to examine temporal differences between prosaccade and antisaccade trials in brain regions associated with saccade control. For stimulus‐aligned antisaccade trials, a longer SRT was associated with delayed onset of neural activity within the ipsilateral parietal eye field (PEF) and bilateral frontal eye field (FEF). Saccade‐aligned activity demonstrated peak activation 10ms before saccade‐onset within the contralateral PEF for prosaccade trials and within the bilateral FEF for antisaccade trials. In addition, failure to inhibit prosaccades on anti‐saccade trials was associated with increased activity prior to saccade onset within the FEF contralateral to the peripheral stimulus. This work on dynamic activity adds to our knowledge that direction errors were due, at least in part, to a failure to inhibit automatic prosaccades. These findings provide novel evidence in humans regarding the temporal dynamics within oculomotor areas needed for saccade programming and the role frontal brain regions have on top‐down inhibitory control.