Corticokinematic coherence mainly reflects movement-induced proprioceptive feedback

Abstract

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.

Keywords: Human brain; Kinematics; Magnetoencephalography; Movement; Partial directed coherence; Proprioception; Sensorimotor cortex.

Fig. 1

Fixed-pace experiment: coherence spectra and directionality results. A. Coherence spectra (one trace per subject) and associated group-level topographic distribution at F0, F1, and averaged across F0 and F1. B. Renormalized partial directed coherence (rPDC) in the afferent and efferent directions (one trace per subject). C. Same as B with added noise to the accelerometer (Acc) signal. The gray horizontal lines indicate the threshold of statistical significance. SM1: primary sensorimotor.

Fig. 2

Fixed-pace experiment: rPDC values (mean and SEM) between primary sensorimotor (SM1) and acceleration (Acc) signals, for all conditions, and in both noise configurations (noiseless and noisy Acc) 9 p-values of paired t-tests comparing the afferent and efferent rPDC are shown on top of the rPDC values.

Fig. 3

Variable-pace experiment: coherence spectra and directionality results. A (active) and C (passive): Coherence spectra and associated topographic distribution in the frequency range of significant coherence. B (active) and D (passive): Renormalized partial directed coherence (rPDC). The smaller insets display the phase–frequency plots of the Fourier coefficients of the multivariate autoregressive model, which were used to estimate the delay through linear regression (red line). The gray horizontal lines indicate the threshold of statistical significance. Acc: accelerometer. SM1: primary sensorimotor.