James E. Gehringer

Oscillatory dynamics and functional connectivity during gating of primary somatosensory responses

Sensory gating is important for preventing excessive environmental stimulation from overloading neural resources. Gating in the human somatosensory cortices is a critically understudied topic, particularly in the lower extremities. We utilize the unique capabilities of magnetoencephalographic neuroimaging to quantify the normative neural population responses and dynamic functional connectivity of somatosensory gating in the lower extremities of healthy human participants. We show that somatosensory processing is subserved by a robust gating effect in the oscillatory domain, as well as a dynamic effect on interhemispheric functional connectivity between primary sensory cortices. These results provide novel insight into the dynamic neural mechanisms that underlie the processing of somatosensory information in the human brain, and will be vital in better understanding the neural responses that are aberrant in gait‐related neurological disorders (e.g. cerebral palsy).

Developmental Trajectory of Beta Cortical Oscillatory Activity During a Knee Motor Task

There is currently a void in the scientific literature on the cortical beta oscillatory activity that is associated with the production of leg motor actions. In addition, we have limited data on how these cortical oscillations may progressively change as a function of development. This study began to fill this vast knowledge gap by using high-density magnetoencephalography to quantify the beta cortical oscillatory activity over a cross-section of typically developing children as they performed an isometric knee target matching task. Advanced beamforming methods were used to identify the spatiotemporal changes in beta oscillatory activity during the motor planning and motor action time frames. Our results showed that a widespread beta event-related desynchronization (ERD) was present across the pre/postcentral gyri, supplementary motor area, and the parietal cortices during the motor planning stage. The strength of this beta ERD sharply diminished across this fronto-parietal network as the children initiated the isometric force needed to match the target. Rank order correlations indicated that the older children were more likely to initiate their force production sooner, took less time to match the targets, and tended to have a weaker beta ERD during the motor planning stage. Lastly, we determined that there was a relationship between the child’s age and the strength of the beta ERD within the parietal cortices during isometric force production. Altogether our results suggest that there are notable maturational changes during childhood and adolescence in beta cortical oscillatory activity that are associated with the planning and execution of leg motor actions.

A reduced somatosensory gating response in individuals with multiple sclerosis is related to walking impairment

When identical stimuli are presented in rapid temporal succession, neural responses to the second stimulation are often weaker than those observed for the first. This phenomenon is termed sensory gating and is believed to be an adaptive feature that helps prevent higher-order cortical centers from being flooded with unnecessary information. Recently, sensory gating in the somatosensory system has been linked to deficits in tactile discrimination. Additionally, studies have linked poor tactile discrimination with impaired walking and balance in individuals with multiple sclerosis (MS). In this study, we examine the neural basis of somatosensory gating in patients with MS and healthy controls and assess the relationship between somatosensory gating and walking performance. We used magnetoencephalography to record neural responses to paired-pulse electrical stimulation applied to the right posterior tibial nerve. All participants also walked across a digital mat, which recorded their spatiotemporal gait kinematics. Our results showed the amplitude of the response to the second stimulation was sharply reduced only in controls, resulting in a significantly reduced somatosensory gating in the patients with MS. No group differences were observed in the amplitude of the response to the first stimulation nor the latency of the neural response to either the first or second stimulation. Interestingly, the altered somatosensory gating responses were correlated with aberrant spatiotemporal gait kinematics in the patients with MS. These results suggest that inhibitory GABA circuits may be altered in patients with MS, which impacts somatosensory gating and contributes to the motor performance deficits seen in these patients.NEW & NOTEWORTHY We aimed to determine whether somatosensory gating in patients with multiple sclerosis (MS) differed compared with healthy controls and whether a relationship exists between somatosensory gating and walking performance. We found reduced somatosensory gating responses in patients with MS, and these altered somatosensory gating responses were correlated with the mobility impairments. These novel findings show that somatosensory gating is impaired in patients with MS and is related to the mobility impairments seen in these patients.

Altered sensorimotor cortical oscillations in individuals with multiple sclerosis suggests a faulty internal model

Multiple sclerosis (MS) is a demyelinating disease that results in a broad array of symptoms, including impaired motor performance. How such demyelination of fibers affects the inherent neurophysiological activity in motor circuits, however, remains largely unknown. Potentially, the movement errors associated with MS may be due to imperfections in the internal model used to make predictions of the motor output that will meet the task demands. Prior magnetoencephalographic (MEG) and electroencephalographic brain imaging experiments have established that the beta (15‐30 Hz) oscillatory activity in the sensorimotor cortices is related to the control of movement. Specifically, it has been suggested that the strength of the post‐movement beta rebound may indicate the certainty of the internal model. In this study, we used MEG to evaluate the neural oscillatory activity in the sensorimotor cortices of individuals with MS and healthy individuals during a goal‐directed isometric knee force task. Our results showed no difference between the individuals with MS and healthy individuals in the beta activity during the planning and execution stages of movement. However, we did find that individuals with MS exhibited a weaker post‐movement beta rebound in the pre/postcentral gyri relative to healthy controls. Additionally, we found that the behavioral performance of individuals with MS was aberrant, and related to the strength of the post‐movement beta rebound. These results suggest that the internal model may be faulty in individuals with MS. Hum Brain Mapp 38:4009–4018, 2017.

Children with cerebral palsy have altered oscillatory activity in the motor and visual cortices during a knee motor task

The neuroimaging literature on cerebral palsy (CP) has predominantly focused on identifying structural aberrations within the white matter (e.g., fiber track integrity), with very few studies examining neural activity within the key networks that serve the production of motor actions. The current investigation used high-density magnetoencephalography to begin to fill this knowledge gap by quantifying the temporal dynamics of the alpha and beta cortical oscillations in children with CP (age = 15.5 ± 3 years; GMFCS levels II–III) and typically developing (TD) children (age = 14.1 ± 3 years) during a goal-directed isometric target-matching task using the knee joint. Advanced beamforming methods were used to image the cortical oscillations during the movement planning and execution stages. Compared with the TD children, our results showed that the children with CP had stronger alpha and beta event-related desynchronization (ERD) within the primary motor cortices, premotor area, inferior parietal lobule, and inferior frontal gyrus during the motor planning stage. Differences in beta ERD amplitude extended through the motor execution stage within the supplementary motor area and premotor cortices, and a stronger alpha ERD was detected in the anterior cingulate. Interestingly, our results also indicated that alpha and beta oscillations were weaker in the children with CP within the occipital cortices and visual MT area during movement execution. These altered alpha and beta oscillations were accompanied by slower reaction times and substantial target matching errors in the children with CP. We also identified that the strength of the alpha and beta ERDs during the motor planning and execution stages were correlated with the motor performance. Lastly, our regression analyses suggested that the beta ERD within visual areas during motor execution primarily predicted the amount of motor errors. Overall, these data suggest that uncharacteristic alpha and beta oscillations within visuomotor cortical networks play a prominent role in the atypical motor actions exhibited by children with CP.

Age-related differences in the motor planning of a lower leg target matching task

While the development and execution of upper extremity motor plans have been well explored, little is known about how individuals plan and execute rapid, goal-directed motor tasks with the lower extremities. Furthermore, the amount of time needed to integrate the proper amount of visual and proprioceptive feedback before being able to accurately execute a goal-directed movement is not well understood; especially in children. Therefore, the purpose of this study was to initially interrogate how the amount of motor planning time provided to a child before movement execution may influence the preparation and execution of a lower leg goal-directed movement. The results displayed that the amount of pre-movement motor planning time provided may influence the reaction time and accuracy of a goal directed leg movement. All subjects in the study had longer reaction times and less accurate movements when no pre-movement motor planning time was provided. In addition, the children had slower reaction times, slower movements, and less accurate movements than the adults for all the presented targets and motor planning times. These results highlight that children may require more time to successfully plan a goal directed movement with the lower extremity. This suggests that children may potentially have less robust internal models than adults for these types of motor skills.

Neurophysiological changes in the visuomotor network after practicing a motor task

Although it is well appreciated that practicing a motor task updates the associated internal model, it is still unknown how the cortical oscillations linked with the motor action change with practice. The present study investigates the short-term changes (e.g., fast motor learning) in the α- and β-event-related desynchronizations (ERD) associated with the production of a motor action. To this end, we used magnetoencephalography to identify changes in the α- and β-ERD in healthy adults after participants practiced a novel isometric ankle plantarflexion target-matching task. After practicing, the participants matched the targets faster and had improved accuracy, faster force production, and a reduced amount of variability in the force output when trying to match the target. Parallel with the behavioral results, the strength of the β-ERD across the motor-planning and execution stages was reduced after practice in the sensorimotor and occipital cortexes. No pre/postpractice changes were found in the α-ERD during motor planning or execution. Together, these outcomes suggest that fast motor learning is associated with a decrease in β-ERD power. The decreased strength likely reflects a more refined motor plan, a reduction in neural resources needed to perform the task, and/or an enhancement of the processes that are involved in the visuomotor transformations that occur before the onset of the motor action. These results may augment the development of neurologically based practice strategies and/or lead to new practice strategies that increase motor learning. NEW & NOTEWORTHY We aimed to determine the effects of practice on the movement-related cortical oscillatory activity. Following practice, we found that the performance of the ankle plantarflexion target-matching task improved and the power of the β-oscillations decreased in the sensorimotor and occipital cortexes. These novel findings capture the β-oscillatory activity changes in the sensorimotor and occipital cortexes that are coupled with behavioral changes to demonstrate the effects of motor learning.

Movement-Related Somatosensory Activity Is Altered in Patients with Multiple Sclerosis.

During active movement the somatosensory cortical responses are often attenuated. This attenuation is referred to as movement-related sensory gating. It is well known that patients with multiple sclerosis (MS) have sensory processing deficits, and recent work has also suggested that these patients display impaired motor control of the ankle musculature. The primary goal of the current study was to: (1) examine the movement-related somatosensory gating in patients with MS and demographically-matched controls, and (2) identify the relationship between the sensory gating and motor control of the ankle musculature. To this end, we used magnetoencephalography brain imaging to assess the neural responses to a tibial nerve electrical stimulation that was applied at rest (passive) and during an ankle plantarflexion motor task (active condition). All participants also completed an ankle isometric motor control task that was performed outside the scanner. Our results indicated that the controls, but not patients with MS, exhibited significantly reduced somatosensory responses during the active relative to passive conditions, and that patients with MS had stronger responses compared with controls during the active condition. Additionally, control of the ankle musculature was related to the extent of movement-related sensory attenuation, with poor motor control being associated with reduced gating. Overall, these results show that patients with MS do not attenuate the somatosensory cortical activity during motor actions, and that the inability to modulate somatosensory cortical activity is partially related to the poor ankle motor control seen in these patients.

Dissipation of disturbances seen in the knee joint kinematics of children with cerebral palsy.

PURPOSE Children with cerebral palsy (CP) often use a crouch gait pattern that has disturbances in the knee joint kinematics. Although the length and rate of lengthening of the hamstring musculature have been speculated to be the reason that these disturbances are not adequately dissipated, this relationship has not been adequately explored. The purpose of this exploratory investigation was to use simulations of a musculoskeletal model and Floquet analysis to evaluate how the performance of hamstrings musculature during gait may be related to the knee joint instabilities seen in children with CP. METHODS Children with CP and typically developing (TD) children walked on a treadmill as a motion capture system assessed the knee joint kinematics. Floquet analysis was used to quantify the rate that disturbances present at the knee joint were dissipated, and simulations of a musculoskeletal model were used to estimate the in vivo length and velocity of the hamstrings. Pearson correlation coefficients were calculated to determine if there was a relationship between the rate that the disturbances were dissipated and the performance of the hamstring musculature. RESULTS The children with CP had hamstrings that lengthened more slowly than TD children, and required more strides to dissipate disturbances in the knee joint kinematics. There was negative correlation between the rate that the hamstrings lengthened and the rate that the knee joint disturbances were dissipated. CONCLUSIONS Our results suggest that the ability of children with CP to dissipate the knee joint disturbances may be related to the inability to properly control the hamstring musculature.