For vision, audition and tactile sense, the optimal stimulus frequency for fMRI is somewhat known. For proprioception, i.e., the “movement sense”, however, the optimal frequency is unknown. We studied the effect of passive-finger-movement frequency on proprioceptive fMRI responses using a novel pneumatic-movement actuator. Eleven healthy right-handed volunteers participated in the study. The movement actuator passively moved the participant’s right index finger at frequencies of 0.3, 1, 3, 6, 9, or 12 Hz in a blocked design. A functional localizer was used to define regions-of-interest in SI and SII cortices. In addition, effect of movement range on the fMRI responses was tested in a separate session with 1, 3, 5, and 7 mm movement ranges at a fixed 2 Hz frequency. In primary somatosensory (SI) cortex, the responses were stronger at 3 Hz than at 0.3 Hz (p < 0.001) or 1 Hz (p < 0.05), and at ≥6 Hz than 0.3 Hz (p < 0.001 for frequencies ≥ 6 Hz). In secondary somatosensory (SII) cortex, all movements, except at 0.3 Hz, elicited significant responses of similar strength. In addition, 6, 9, and 12-Hz movements elicited a significant offset response in both SI and SII cortices (p < 0.001–0.05). SI cortex required a total stimulation duration of 4 min to elicit significant activations at the group-level whereas for SII cortex 1 min 20 s was sufficient. Increase in the movement range led to stronger responses in SI cortex, but not in SII cortex. Movements above 3 Hz elicited the strongest SI cortex responses, and increase in the movement range enhanced the response strength. We thus recommend that movements at 3–6 Hz with a movement range of 5 mm or higher to be used in future studies of proprioception. Our results are in-line with previous fMRI and PET studies using tactile or median nerve stimulation at different stimulation frequencies.

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 inter-stimulus 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 yrs, 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 was collected. Finger kinematics were recorded with a 3-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.

Graphical abstract

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.

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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.

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