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Publisher Copyright: © The Author(s) 2022. Published by Oxford University Press. 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.

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

Funding Information: This study has been supported by the Academy of Finland ”Brain changes across the life‐span” profiling funding to University of Jyväskylä (grant #311877). HP was supported by Academy of Finland (grants #296240, #326988, #307250 and #327288) to HP and Jane and Aatos Erkko Foundation (grant #602.274). Publisher Copyright: © 2021 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd. Copyright: Copyright 2021 Elsevier B.V., All rights reserved. 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.

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.

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.