More comprehensive proprioceptive stimulation of the hand amplifies its cortical processing

Abstract

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.

Keywords: acceleration; corticokinematic coherence; magnetoencephalography; proprioception; sensorimotor cortex.

Graphical abstract

Figure 1.

Proprioceptive stimulator, sustained-MEG fields for each finger, and acceleration magnitude for the index finger. A: the four-finger proprioceptive stimulator. Please note that the figure is only for visualization purposes and does not include all four accelerometers. B–D: averaged MEG responses (vector sum of the peak gradiometer pair) for each finger and acceleration magnitude (Euclidean norm of the three orthogonal components) for the index finger in all three conditions. The red dashed line indicates an onset of the flexion phase of the continuous flexion-extension movement. MEG, magnetoencephalography.

Figure 2.

CKC strength for all conditions at the source level. A: average CKC strength for separate versus simultaneous stimulation at 3 Hz (left) and separate versus simultaneous stimulation at finger-specific frequencies. B: CKC strength for individual fingers when stimulated separately versus simultaneously at 3 Hz. C: CKC strength for individual fingers when stimulated separately versus simultaneously at finger-specific frequencies. Statistical differences were computed using a two-way repeated measurements analysis of variances.*P < 0.05, **P < 0.01, ***P < 0.001. CKC, corticokinematic coherence; N, number of subjects.

Figure 3.

CKC strength for individual fingers at the source level. Average CKC for the separate stimulation of individual fingers (A) and for the simultaneous stimulation at the fingers at their specific frequencies (B). Statistical differences were computed using a two-way repeated measurements analysis of variances. *P < 0.05. CKC, corticokinematic coherence; N, number of participants.

Figure 4.

CKC-source-peak locations. A: group-level CKC source locations of each finger overlaid on the same volumetric brain (top) and cortical surface (bottom) separately for each condition. Please note that x-coordinates are averages over the x-directional MNI coordinates of the CKC source locations of the four fingers (for the MNI source coordinates of each finger, see Table 3). B: CKC source locations of each finger of four representative participants (S1–S4) overlaid on the same cortical surface separately for each condition. C: group-level CKC source locations of each condition overlaid on the same cortical surface separately for each finger. Please note that the source locations were concentrated on the Rolandic hand region of the SM1 cortex (i.e., central sulcus) in the source volume, but were misleadingly projected away from the central sulcus in the anterior wall of the postcentral sulcus when visualized to the cortical surface. CKC, corticokinematic coherence; N, number of participants.