Volitional muscle activation intensifies neuronal processing of proprioceptive afference in the primary sensorimotor cortex: an EEG study.

Proprioception refers to the ability to perceive the position and movement of body segments in space. The cortical aspects of the proprioceptive afference from the body can be investigated using corticokinematic coherence (CKC). CKC accurately quantifies the degree of coupling between cortical activity and limb kinematics, especially if precise proprioceptive stimulation of evoked movements is used. However, there is no evidence on how volitional muscle activation during proprioceptive stimulation affects CKC strength. Twenty-five healthy volunteers (28.8 ± 7 yr, 11 females) participated in the experiment, which included electroencephalographic (EEG), electromyographic (EMG), and kinematic recordings. Ankle-joint rotations (2-Hz) were elicited through a movement actuator in two conditions: passive condition with relaxed ankle and active condition with constant 5-Nm plantar flexion exerted during the stimulation. In total, 6 min of data were recorded per condition. CKC strength was defined as the maximum coherence value among all the EEG channels at the 2-Hz movement frequency for each condition separately. Both conditions resulted in significant CKC peaking at the Cz electrode over the foot area of the primary sensorimotor (SM1) cortex. Stronger CKC was found for the active (0.13 ± 0.14) than the passive (0.03 ± 0.04) condition (P < 0.01). The results indicated that volitional activation of the muscles intensifies the neuronal proprioceptive processing in the SM1 cortex. This finding could be explained both by peripheral sensitization of the ankle joint proprioceptors and central modulation of the neuronal proprioceptive processing at the spinal and cortical levels.NEW & NOTEWORTHY The current study is the first to investigate the effect of volitional muscle activation on CKC-based assessment of cortical proprioception of the ankle joint. Results show that the motor efference intensifies the neuronal processing of proprioceptive afference of the ankle joint. This is a significant finding as it may extend the use of CKC method during active tasks to further evaluate the motor efference-proprioceptive afference relationship and the related adaptations to exercise, rehabilitation, and disease.

Limb-specific thalamocortical tracts are impaired differently in hemiplegic and diplegic subtypes of cerebral palsy.

Thalamocortical pathways are considered crucial in the sensorimotor functioning of children with cerebral palsy (CP). However, previous research has been limited by non-specific tractography seeding and the lack of comparison between different CP subtypes. We compared limb-specific thalamocortical tracts between children with hemiplegic (HP, N = 15) or diplegic (DP, N = 10) CP and typically developed peers (N = 19). The cortical seed-points for the upper and lower extremities were selected (i) manually based on anatomical landmarks or (ii) using functional magnetic resonance imaging (fMRI) activations following proprioceptive-limb stimulation. Correlations were investigated between tract structure (mean diffusivity, MD; fractional anisotropy, FA; apparent fiber density, AFD) and sensorimotor performance (hand skill and postural stability). Compared to controls, our results revealed increased MD in both upper and lower limb thalamocortical tracts in the non-dominant hemisphere in HP and bilaterally in DP subgroup. MD was strongly lateralized in participants with hemiplegia, while AFD seemed lateralized only in controls. fMRI-based tractography results were comparable. The correlation analysis indicated an association between the white matter structure and sensorimotor performance. These findings suggest distinct impairment of functionally relevant thalamocortical pathways in HP and DP subtypes. Thus, the organization of thalamocortical white matter tracts may offer valuable guidance for targeted, life-long rehabilitation in children with CP.

Cortical networks show characteristic recruitment patterns after somatosensory stimulation by pneumatically evoked repetitive hand movements in newborn infants.

Controlled assessment of functional cortical networks is an unmet need in the clinical research of noncooperative subjects, such as infants. We developed an automated, pneumatic stimulation method to actuate naturalistic movements of an infant's hand, as well as an analysis pipeline for assessing the elicited electroencephalography (EEG) responses and related cortical networks. Twenty newborn infants with perinatal asphyxia were recruited, including 7 with mild-to-moderate hypoxic-ischemic encephalopathy (HIE). Statistically significant corticokinematic coherence (CKC) was observed between repetitive hand movements and EEG in all infants, peaking near the contralateral sensorimotor cortex. CKC was robust to common sources of recording artifacts and to changes in vigilance state. A wide recruitment of cortical networks was observed with directed phase transfer entropy, also including areas ipsilateral to the stimulation. The extent of such recruited cortical networks was quantified using a novel metric, Spreading Index, which showed a decrease in 4 (57%) of the infants with HIE. CKC measurement is noninvasive and easy to perform, even in noncooperative subjects. The stimulation and analysis pipeline can be fully automated, including the statistical evaluation of the cortical responses. Therefore, the CKC paradigm holds great promise as a scientific and clinical tool for controlled assessment of functional cortical networks.

Proprioceptive response strength in the primary sensorimotor cortex is invariant to the range of finger movement.

Proprioception is the sense of body position and movement that relies on afference from the proprioceptors in muscles and joints. Proprioceptive responses in the primary sensorimotor (SM1) cortex can be elicited by stimulating the proprioceptors using evoked (passive) limb movements. In magnetoencephalography (MEG), proprioceptive processing can be quantified by recording the movement evoked fields (MEFs) and movement-induced beta power modulations or by computing corticokinematic coherence (CKC) between the limb kinematics and cortical activity. We examined whether cortical proprioceptive processing quantified with MEF peak strength, relative beta suppression and rebound power and CKC strength is affected by the movement range of the finger. MEG activity was measured from 16 right-handed healthy volunteers while movements were applied to their right-index finger metacarpophalangeal joint with an actuator. Movements were either intermittent, every 3000 ± 250 ms, to estimate MEF or continuous, at 3 Hz, to estimate CKC. In both cases, 4 different ranges of motion of the stimuli were investigated: 15, 18, 22 and 26 mm for MEF and 6, 7, 9 and 13 mm for CKC. MEF amplitude, relative beta suppression and rebound as well as peak CKC strength at the movement frequency were compared between the movement ranges in the source space. Inter-individual variation was also compared between the MEF and CKC strengths. As expected, MEF and CKC responses peaked at the contralateral SM1 cortex. MEF peak, beta suppression and rebound and CKC strengths were similar across all movement ranges. Furthermore, CKC strength showed a lower degree of inter-individual variation compared with MEF strength. Our result of absent modulation by movement range in cortical responses to passive movements of the finger indicates that variability in movement range should not hinder comparability between different studies or participants. Furthermore, our data indicates that CKC is less prone to inter-individual variability than MEFs, and thus more advantageous in what pertains to statistical power.

Identification of proprioceptive thalamocortical tracts in children: comparison of fMRI, MEG, and manual seeding of probabilistic tractography.

Studying white matter connections with tractography is a promising approach to understand the development of different brain processes, such as proprioception. An emerging method is to use functional brain imaging to select the cortical seed points for tractography, which is considered to improve the functional relevance and validity of the studied connections. However, it is unknown whether different functional seeding methods affect the spatial and microstructural properties of the given white matter connection. Here, we compared functional magnetic resonance imaging, magnetoencephalography, and manual seeding of thalamocortical proprioceptive tracts for finger and ankle joints separately. We showed that all three seeding approaches resulted in robust thalamocortical tracts, even though there were significant differences in localization of the respective proprioceptive seed areas in the sensorimotor cortex, and in the microstructural properties of the obtained tracts. Our study shows that the selected functional or manual seeding approach might cause systematic biases to the studied thalamocortical tracts. This result may indicate that the obtained tracts represent different portions and features of the somatosensory system. Our findings highlight the challenges of studying proprioception in the developing brain and illustrate the need for using multimodal imaging to obtain a comprehensive view of the studied brain process.

Temporally stable beta sensorimotor oscillations and corticomuscular coupling underlie force steadiness.

As humans, we seamlessly hold objects in our hands, and may even lose consciousness of these objects. This phenomenon raises the unsettled question of the involvement of the cerebral cortex, the core area for voluntary motor control, in dynamically maintaining steady muscle force. To address this issue, we measured magnetoencephalographic brain activity from healthy adults who maintained a steady pinch grip. Using a novel analysis approach, we uncovered fine-grained temporal modulations in the beta sensorimotor brain rhythm and its coupling with muscle activity, with respect to several aspects of muscle force (rate of increase/decrease or plateauing high/low). These modulations preceded changes in force features by ∼40 ms and possessed behavioral relevance, as less salient or absent modulation predicted a more stable force output. These findings have consequences for the existing theories regarding the functional role of cortico-muscular coupling, and suggest that steady muscle contractions are characterized by a stable rather than fluttering involvement of the sensorimotor cortex.

More comprehensive proprioceptive stimulation of the hand amplifies its cortical processing.

Corticokinematic coherence (CKC) quantifies the phase coupling between limb kinematics and cortical neurophysiological signals reflecting proprioceptive feedback to the primary sensorimotor (SM1) cortex. We studied whether the CKC strength or cortical source location differs between proprioceptive stimulation (i.e., actuator-evoked movements) of right-hand digits (index, middle, ring, and little). Twenty-one volunteers participated in magnetoencephalography measurements during which three conditions were tested: 1) simultaneous stimulation of all four fingers at the same frequency, 2) stimulation of each finger separately at the same frequency, and 3) simultaneous stimulation of the fingers at finger-specific frequencies. CKC was computed between MEG responses and accelerations of the fingers recorded with three-axis accelerometers. CKC was stronger (P < 0.003) for the simultaneous (0.52 ± 0.02) than separate (0.45 ± 0.02) stimulation at the same frequency. Furthermore, CKC was weaker (P < 0.03) for the simultaneous stimulation at the finger-specific frequencies (0.38 ± 0.02) than for the separate stimulation. CKC source locations of the fingers were concentrated in the hand region of the SM1 cortex and did not follow consistent finger-specific somatotopic order. Our results indicate that proprioceptive afference from the fingers is processed in partly overlapping cortical neuronal circuits, which was demonstrated by the modulation of the finger-specific CKC strengths due to proprioceptive afference arising from simultaneous stimulation of the other fingers of the same hand as well as overlapping cortical source locations. Finally, comprehensive simultaneous proprioceptive stimulation of the hand would optimize functional cortical mapping to pinpoint the hand region, e.g., prior brain surgery.NEW & NOTEWORTHY Corticokinematic coherence (CKC) can be used to study cortical proprioceptive processing and localize proprioceptive hand representation. Our results indicate that proprioceptive stimulation delivered simultaneously at the same frequency to fingers (D2-D4) maximizes CKC strength allowing robust and fast localization of the human hand region in the sensorimotor cortex using MEG.

Reproducibility of Rolandic beta rhythm modulation in MEG and EEG.

The Rolandic beta rhythm, at ∼20 Hz, is generated in the somatosensory and motor cortices and is modulated by motor activity and sensory stimuli, causing a short lasting suppression that is followed by a rebound of the beta rhythm. The rebound reflects inhibitory changes in the primary sensorimotor (SMI) cortex, and thus it has been used as a biomarker to follow the recovery of patients with acute stroke. The longitudinal stability of beta rhythm modulation is a prerequisite for its use in long-term follow-ups. We quantified the reproducibility of beta rhythm modulation in healthy subjects in a 1-year-longitudinal study both for MEG and EEG at T0, 1 month (T1-month, n = 8) and 1 year (T1-year, n = 19). The beta rhythm (13-25 Hz) was modulated by fixed tactile and proprioceptive stimulations of the index fingers. The relative peak strengths of beta suppression and rebound did not differ significantly between the sessions, and intersession reproducibility was good or excellent according to intraclass correlation-coefficient values (0.70-0.96) both in MEG and EEG. Our results indicate that the beta rhythm modulation to tactile and proprioceptive stimulation is well reproducible within 1 year. These results support the use of beta modulation as a biomarker in long-term follow-up studies, e.g., to quantify the functional state of the SMI cortex during rehabilitation and drug interventions in various neurological impairments.NEW & NOTEWORTHY The present study demonstrates that beta rhythm modulation is highly reproducible in a group of healthy subjects within a year. Hence, it can be reliably used as a biomarker in longitudinal follow-up studies in different neurological patient groups to reflect changes in the functional state of the sensorimotor cortex.

Gating Patterns to Proprioceptive Stimulation in Various Cortical Areas: An MEG Study in Children and Adults using Spatial ICA.

Proprioceptive paired-stimulus paradigm was used for 30 children (10-17 years) and 21 adult (25-45 years) volunteers in magnetoencephalography (MEG). Their right index finger was moved twice with 500-ms interval every 4 ± 25 s (repeated 100 times) using a pneumatic-movement actuator. Spatial-independent component analysis (ICA) was applied to identify stimulus-related components from MEG cortical responses. Clustering was used to identify spatiotemporally consistent components across subjects. We found a consistent primary response in the primary somatosensory (SI) cortex with similar gating ratios of 0.72 and 0.69 for the children and adults, respectively. Secondary responses with similar transient gating behavior were centered bilaterally in proximity of the lateral sulcus. Delayed and prolonged responses with strong gating were found in the frontal and parietal cortices possibly corresponding to larger processing network of somatosensory afference. No significant correlation between age and gating ratio was found. We confirmed that cortical gating to proprioceptive stimuli is comparable to other somatosensory and auditory domains, and between children and adults. Gating occurred broadly beyond SI cortex. Spatial ICA revealed several consistent response patterns in various cortical regions which would have been challenging to detect with more commonly applied equivalent current dipole or distributed source estimates.

Effect of childhood developmental coordination disorder on adulthood physical activity; Arvo Ylppö longitudinal study.

Individuals at risk of Developmental Coordination Disorder (DCD) have low levels of physical activity in childhood due to impaired motor competence; however, physical activity levels in adulthood have not been established. This study sought to determine the impact of DCD risk on physical activity levels in adults using accelerometry measurement. Participants (n = 656) from the Arvo Ylppö Longitudinal Study cohort had their motor competence assessed at the age of five years, and their physical activity quantified via device assessment at the age of 25 years. Between group differences were assessed to differentiate physical activity measures for individuals based on DCD risk status, with general linear modeling performed to control for the effects of sex, body mass index (BMI), and maternal education. Participants at risk of DCD were found to have a lower total number of steps (d = 0.3, p = 0.022) than those not at risk. Statistical modeling indicated that DCD risk status increased time spent in sedentary light activity (ß = 0.1, 95% CI 0.02 to 0.3, p = 0.026) and decreased time spent in vigorous physical activity via interaction with BMI (ß = 0.04, 95% CI 0.001 to 0.1, p = 0.025). Sensitivity analysis found that visuomotor impairment did not significantly impact physical activity but did increase the role of DCD risk status in some models. This 20-year-longitudinal study indicated that DCD risk status continues to negatively impact on levels of physical activity into early adulthood.

Corticokinematic coherence is stronger to regular than irregular proprioceptive stimulation of the hand.

Proprioceptive afference can be investigated using corticokinematic coherence (CKC), which indicates coupling between limb kinematics and cortical activity. CKC has been quantified using proprioceptive stimulation (movement actuators) with fixed interstimulus interval (ISI). However, it is unclear how regularity of the stimulus sequence (jitter) affects CKC strength. Eighteen healthy volunteers (16 right-handed, 27.8 ± 5.0 yr, 7 females) participated in magnetoencephalography (MEG) session in which their right index finger was continuously moved at ∼3 Hz with Constant 333 ms ISI or with 20% Jitter (ISI 333 ± 66 ms) using a pneumatic-movement actuator. Three minutes of data per condition were collected. Finger kinematics were recorded with a three-axis accelerometer. CKC strength was defined as the peak coherence value in the Rolandic MEG gradiometer pair contralateral to the movement at 3 Hz. Both conditions resulted in significant coherence peaking in the gradiometers over the primary sensorimotor cortex. Constant stimulation yielded stronger CKC at 3 Hz (0.78 ± 0.11 vs. 0.66 ± 0.13, P < 0.001) and its first harmonic (0.60 ± 0.19 vs. 0.27 ± 0.11, P < 0.001) than irregular stimulation. Similarly, the respective sustained-movement evoked field was also stronger for constant stimulation. The results emphasize the importance of temporal stability of the proprioceptive stimulation sequence when quantifying CKC strength. The weaker CKC during irregular stimulation can be explained with temporal and thus spectral scattering of the paired peripheral and cortical events beyond the mean stimulation frequency. This impairs the signal-to-noise ratio of respective MEG signal and thus CKC strength. When accurately estimating and following changes in CKC strength, we suggest using precise movement actuators with constant stimulation sequence.NEW & NOTEWORTHY Cortical proprioceptive processing can be investigated using corticokinematic coherence (CKC). The findings show that CKC method is sensitive to temporal stability in the stimulation sequence. Although both regular and irregular sequences resulted in robust coherence, the regular stimulation sequence with pneumatic movement actuator is recommended to maximize coherence strength and reproducibility to allow better comparability between groups or populations.

Attention directed to proprioceptive stimulation alters its cortical processing in the primary sensorimotor cortex.

Movement-evoked fields to passive movements and corticokinematic coherence between limb kinematics and magnetoencephalographic signals can both be used to quantify the degree of cortical processing of proprioceptive afference. We examined in 20 young healthy volunteers whether processing of proprioceptive afference in the primary sensorimotor cortex is modulated by attention directed to the proprioceptive stimulation of the right index finger using a pneumatic-movement actuator to evoke continuous 3-Hz movement for 12 min. The participant attended either to a visual (detected change of fixation cross colour) or movement (detected missing movements) events. The attentional task alternated every 3-min. Coherence was computed between index-finger acceleration and magnetoencephalographic signals, and sustained-movement-evoked fields were averaged with respect to the movement onsets every 333 ms. Attention to the proprioceptive stimulation supressed the sensorimotor beta power (by ~12%), enhanced movement-evoked field amplitude (by ~16%) and reduced corticokinematic coherence strength (by ~9%) with respect to the visual task. Coherence peaked at the primary sensorimotor cortex contralateral to the proprioceptive stimulation. Our results indicated that early processing of proprioceptive afference in the primary sensorimotor cortex is modulated by inter-modal directed attention in healthy individuals. Therefore, possible attentional effects on corticokinematic coherence and movement-evoked fields should be considered when using them to study cortical proprioception in conditions introducing attentional variation.

Comparing MEG and EEG in detecting the ~20-Hz rhythm modulation to tactile and proprioceptive stimulation.

Modulation of the ~20-Hz brain rhythm has been used to evaluate the functional state of the sensorimotor cortex both in healthy subjects and patients, such as stroke patients. The ~20-Hz brain rhythm can be detected by both magnetoencephalography (MEG) and electroencephalography (EEG), but the comparability of these methods has not been evaluated. Here, we compare these two methods in the evaluating of ~20-Hz activity modulation to somatosensory stimuli. Rhythmic ~20-Hz activity during separate tactile and proprioceptive stimulation of the right and left index finger was recorded simultaneously with MEG and EEG in twenty-four healthy participants. Both tactile and proprioceptive stimulus produced a clear suppression at 300-350 â€‹ms followed by a subsequent rebound at 700-900 â€‹ms after stimulus onset, detected at similar latencies both with MEG and EEG. The relative amplitudes of suppression and rebound correlated strongly between MEG and EEG recordings. However, the relative strength of suppression and rebound in the contralateral hemisphere (with respect to the stimulated hand) was significantly stronger in MEG than in EEG recordings. Our results indicate that MEG recordings produced signals with higher signal-to-noise ratio than EEG, favoring MEG as an optimal tool for studies evaluating sensorimotor cortical functions. However, the strong correlation between MEG and EEG results encourages the use of EEG when translating studies to clinical practice. The clear advantage of EEG is the availability of the method in hospitals and bed-side measurements at the acute phase.

Feasibility and reproducibility of electroencephalography-based corticokinematic coherence.

Corticokinematic coherence (CKC) is the phase coupling between limb kinematics and cortical neurophysiological signals, reflecting cortical processing of proprioceptive afference, and it is reproducible when estimated with magnetoencephalography (MEG). However, feasibility and reproducibility of CKC based on electroencephalography (EEG) is still unclear and is the primary object of the present report. Thirteen healthy right-handed volunteers (seven females, 21.7 ± 4.3 yr) participated in two combined MEG/EEG sessions 12.6 ± 1.3 mo apart. Participants' dominant and nondominant index finger was continuously moved at 3 Hz for 4 min separately using a pneumatic-movement actuator. Coherence was computed between finger acceleration and three derivations of EEG signals: 1) average reference, 2) bipolar derivations, and 3) surface Laplacian. CKC strength was defined as the peak coherence value at movement frequency. Intraclass-correlation coefficient values (0.74-0.93) indicated excellent intersession reproducibility for CKC strength for all derivations and moved fingers. CKC strength obtained with EEG was approximately two times lower compared with MEG, but the values were positively correlated across the participants. CKC strength was significantly (P < 0.01) higher for bipolar (session 1: 0.19 ± 0.09; session 2: 0.20 ± 0.10) and surface Laplacian (session 1: 0.22 ± 0.09; session 2: 0.21 ± 0.09) derivations than for the average reference (session 1: 0.10 ± 0.04; session 2: 0.11 ± 0.05). We demonstrated that CKC is a feasible and reproducible tool to monitor proprioception using EEG recordings, although the strength of CKC was twice lower for EEG compared with MEG. Laplacian and bipolar (CP3-C1/CP3-C3 and CP4-C2/C4-FC2) EEG derivation(s) are recommended for future research and clinical use of CKC method. NEW & NOTEWORTHY The most important message in this report is that the corticokinematic coherence (CKC) method is a feasible and reproducible tool to quantify, map, and follow cortical proprioceptive ("the movement sense") processing using EEG that is more widely available for CKC recordings than previously used magnetoencephalography designs, in basic research, but especially in clinical environments. We provide useful recommendations for optimal EEG derivations for cost-effective experimental designs, making it possible to scale up in sample size in future studies.

Neuromuscular Adaptations to Short-Term High-Intensity Interval Training in Female Ice-Hockey Players.

Kinnunen, J-V, Piitulainen, H, and Piirainen, JM. Neuromuscular adaptations to short-term high-intensity interval training in female ice-hockey players. J Strength Cond Res 33(2): 479-485, 2019-High-intensity interval training (HIIT)-related neuromuscular adaptations, changes in force production, and on-ice performance were investigated in female ice-hockey players during preseason. Fourteen Finnish championship level ice-hockey players (average age 22 ± 3 years) participated in 2½-week HIIT. Both spinal (H-reflex) and supraspinal (V-wave) neuromuscular responses of the soleus muscle were recorded before and after the training period. Static jump (SJ) and countermovement jump heights, plantarflexor maximum voluntary contraction (MVC), and rate of force development (RFD) were measured. In addition, soleus and tibialis anterior muscle activations (electromyography) were measured during MVC and RFD tests. During on-ice training, skating speed and acceleration tests were performed. Subjects significantly improved their plantarflexion MVC force (11.6 ± 11.2%, p < 0.001), RFD (15.2 ± 15.9%, p < 0.01), and SJ (4.8 ± 7.6%, p ≤ 0.05). Voluntary motor drive to the soleus muscle (V-wave amplitude) increased by 16.0 ± 15.4% (p < 0.01), and coactivation of the tibialis anterior muscle during the plantarflexion RFD test was reduced by -18.9 ± 22.2% (p ≤ 0.05). No change was observed in spinal α-motoneuron excitability (H-reflex) during MVC or in on-ice performance. These results indicate that HIIT can be used to improve athletes' capability to produce maximal and explosive forces, likely through enhanced voluntary activation of their muscles and reduced antagonist coactivation. Therefore, HIIT can be recommended in preseason training to improve neuromuscular performance. However, a longer than 2½-week HIIT period is needed to improve on-ice performance in female ice-hockey players.

MEG Insight into the Spectral Dynamics Underlying Steady Isometric Muscle Contraction.

To gain fundamental knowledge on how the brain controls motor actions, we studied in detail the interplay between MEG signals from the primary sensorimotor (SM1) cortex and the contraction force of 17 healthy adult humans (7 females, 10 males). SM1 activity was coherent at ∼20 Hz with surface electromyogram (as already extensively reported) but also with contraction force. In both cases, the effective coupling was dominant in the efferent direction. Across subjects, the level of ∼20 Hz coherence between cortex and periphery positively correlated with the "burstiness" of ∼20 Hz SM1 (Pearson r ≈ 0.65) and peripheral fluctuations (r ≈ 0.9). Thus, ∼20 Hz coherence between cortex and periphery is tightly linked to the presence of ∼20 Hz bursts in SM1 and peripheral activity. However, the very high correlation with peripheral fluctuations suggests that the periphery is the limiting factor. At frequencies <3 Hz, both SM1 signals and ∼20 Hz SM1 envelope were coherent with both force and its absolute change rate. The effective coupling dominated in the efferent direction between (1) force and the ∼20 Hz SM1 envelope and (2) the absolute change rate of the force and SM1 signals. Together, our data favor the view that ∼20 Hz coherence between cortex and periphery during isometric contraction builds on the presence of ∼20 Hz SM1 oscillations and needs not rely on feedback from the periphery. They also suggest that effective cortical proprioceptive processing operates at <3 Hz frequencies, even during steady isometric contractions.SIGNIFICANCE STATEMENT Accurate motor actions are made possible by continuous communication between the cortex and spinal motoneurons, but the neurophysiological basis of this communication is poorly understood. Using MEG recordings in humans maintaining steady isometric muscle contractions, we found evidence that the cortex sends population-level motor commands that tend to structure according to the ∼20 Hz sensorimotor rhythm, and that it dynamically adapts these commands based on the <3 Hz fluctuations of proprioceptive feedback. To our knowledge, this is the first report to give a comprehensive account of how the human brain dynamically handles the flow of proprioceptive information and converts it into appropriate motor command to keep the contraction force steady.

Reproducibility of corticokinematic coherence.

Corticokinematic coherence (CKC) between limb kinematics and magnetoencephalographic (MEG) signals reflects cortical processing of proprioceptive afference. However, it is unclear whether strength of CKC is reproducible across measurement sessions. We thus examined reproducibility of CKC in a follow-up study. Thirteen healthy right-handed volunteers (7 females, 21.7 ±â€¯4.3 yrs) were measured using MEG in two separate sessions 12.6 ±â€¯1.3 months apart. The participant was seated and relaxed while his/her dominant or non-dominant index finger was continuously moved at 3 Hz (4 min for each hand) using a pneumatic movement actuator. Finger kinematics were recorded with a 3-axis accelerometer. Coherence was computed between finger acceleration and MEG signals. CKC strength was defined as the peak coherence value at 3 Hz form a single sensor among 40 pre-selected Rolandic gradiometers contralateral to the movement. Pneumatic movement actuator provided stable proprioceptive stimuli and significant CKC responses peaking at the contralateral Rolandic sensors. In the group level, CKC strength did not differ between the sessions in dominant (Day-1 0.40 ±â€¯0.19 vs. Day-2 0.41 ±â€¯0.17) or non-dominant (0.35 ±â€¯0.16 vs. 0.36 ±â€¯0.17) hand, nor between the hands. Intraclass-correlation coefficient (ICC) values indicated excellent inter-session reproducibility for CKC strength for both dominant (0.86) and non-dominant (0.97) hand. However, some participants showed pronounced inter-session variability in CKC strength, but only for the dominant hand. CKC is a promising tool to study proprioception in long-term longitudinal studies in the group level to follow, e.g., integrity of cortical proprioceptive processing with motor functions after stroke.

Effect of interstimulus interval on cortical proprioceptive responses to passive finger movements.

Shortening of the interstimulus interval (ISI) generally leads to attenuation of cortical sensory responses. For proprioception, however, this ISI effect is still poorly known. Our aim was to characterize the ISI dependence of movement-evoked proprioceptive cortical responses and to find the optimum ISI for proprioceptive stimulation. We measured, from 15 healthy adults, magnetoencephalographic responses to passive flexion and extension movements of the right index finger. The movements were generated by a movement actuator at fixed ISIs of 0.5, 1, 2, 4, 8, and 16 s, in separate blocks. The responses peaked at ~ 70 ms (extension) and ~ 90 ms (flexion) in the contralateral primary somatosensory cortex. The strength of the cortical source increased with the ISI, plateauing at the 8-s ISI. Modeling the ISI dependence with an exponential saturation function revealed response lifetimes of 1.3 s (extension) and 2.2 s (flexion), implying that the maximum signal-to-noise ratio (SNR) in a given measurement time is achieved with ISIs of 1.7 s and 2.8 s respectively. We conclude that ISIs of 1.5-3 s should be used to maximize SNR in recordings of proprioceptive cortical responses to passive finger movements. Our findings can benefit the assessment of proprioceptive afference in both clinical and research settings.

MEG-compatible pneumatic stimulator to elicit passive finger and toe movements.

Magnetoencephalographic (MEG) signals recorded from the primary sensorimotor (SM1) cortex are coherent with kinematics of both active and passive finger movements. The coherence mainly reflects movement-related proprioceptive afference to the cortex. Here we describe a novel MEG-compatible stimulator to generate computer-controlled passive finger and toe movements that can be used as stimuli in functional brain-imaging experiments. The movements are produced by pneumatic artificial muscle (PAM), elastic actuator that shortens with increasing air pressure. To test the applicability of the stimulator to functional brain-imaging, 4-min trains of passive repetitive 5-mm flexion-extension movements of the right and left index finger and the right hallux were produced at 3Hz while the subject's brain activity was measured with whole-scalp MEG and finger or toe kinematics with an accelerometer. In all ten subjects studied, statistically significant coherence (up to 0.78) occurred between the accelerometer and MEG signals at the movement frequency or its first harmonic. Sources of coherent activity were in the contralateral hand or foot SM1 cortices. Movement-evoked fields elicited with intermittent movements of the right index finger (once every 3.2-4.0s; mean±SD peak response latency 88±25ms) were co-located with the respective coherent sources. We further moved the right index finger at 3, 6, and 12Hz (movement ranges 5, 3, and 2mm, respectively), and analyzed the first 1, 2, and 4-min epochs of data. One minute of data was sufficient to locate the left hand area of the SM1 cortex at all movement frequencies. Sound-induced spurious coherence was reliably ruled out in a control experiment. Our novel movement stimulator thus provides a robust and reliable tool to track proprioceptive afference to the cortex and to locate the SM1 cortex.

Corticokinematic coherence mainly reflects movement-induced proprioceptive feedback.

Corticokinematic coherence (CKC) reflects coupling between magnetoencephalographic (MEG) signals and hand kinematics, mainly occurring at hand movement frequency (F0) and its first harmonic (F1). Since CKC can be obtained for both active and passive movements, it has been suggested to mainly reflect proprioceptive feedback to the primary sensorimotor (SM1) cortex. However, the directionality of the brain-kinematics coupling has not been previously assessed and was thus quantified in the present study by means of renormalized partial directed coherence (rPDC). MEG data were obtained from 15 subjects who performed right index-finger movements and whose finger was, in another session, passively moved, with or without tactile input. Four additional subjects underwent the same task with slowly varying movement pace, spanning the 1-5 Hz frequency range. The coupling between SM1 activity recorded with MEG and finger kinematics was assessed with coherence and rPDC. In all conditions, the afferent rPDC spectrum, which resembled the coherence spectrum, displayed higher values than the efferent rPDC spectrum. The afferent rPDC was 37% higher when tactile input was present, and it was at highest at F1 of the passive conditions; the efferent rPDC level did not differ between conditions. The apparent latency for the afferent input, estimated within the framework of the rPDC analysis, was 50-100 ms. The higher directional coupling between hand kinematics and SM1 activity in afferent than efferent direction strongly supports the view that CKC mainly reflects movement-related somatosensory proprioceptive afferent input to the contralateral SM1 cortex.