4.4 Article

More comprehensive proprioceptive stimulation of the hand amplifies its cortical processing

Journal

JOURNAL OF NEUROPHYSIOLOGY
Volume 128, Issue 3, Pages 568-581

Publisher

AMER PHYSIOLOGICAL SOC
DOI: 10.1152/jn.00485.2021

Keywords

acceleration; corticokinematic coherence; magnetoencephalography; proprioception; sensorimotor cortex

Funding

  1. Academy of Finland [296240, 326988, 307250, 327288]
  2. Jane and Aatos Erkko Foundation
  3. Brain changes across the life-span profiling funding [311877]
  4. Finnish Cultural Foundation
  5. Paulo Foundation
  6. Academy of Finland (AKA) [327288] Funding Source: Academy of Finland (AKA)

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Corticokinematic coherence (CKC) analyzes the relationship between limb kinematics and cortical neurophysiological signals. The study found that CKC strength is stronger when all four fingers are simultaneously stimulated at the same frequency, and weaker when fingers are simultaneously stimulated at finger-specific frequencies. The CKC source locations in the cortex are concentrated in the hand region and do not follow a consistent finger-specific somatotopic order. This suggests that proprioceptive feedback from the fingers is processed through partially overlapping neural circuits in the brain.
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 fre-quency to fingers (D2-D4) maximizes CKC strength allowing robust and fast localization of the human hand region in the senso-rimotor cortex using MEG.

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