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.