Unveiling neural coupling within the sensorimotor system: directionality and nonlinearity

Abstract

Neural coupling between the central nervous system and the periphery is essential for the neural control of movement. Corticomuscular coherence is a popular linear technique to assess synchronised oscillatory activity in the sensorimotor system. This oscillatory coupling originates from ascending somatosensory feedback and descending motor commands. However, corticomuscular coherence cannot separate this bidirectionality. Furthermore, the sensorimotor system is nonlinear, resulting in cross-frequency coupling. Cross-frequency oscillations cannot be assessed nor exploited by linear measures. Here, we emphasise the need of novel coupling measures, which provide directionality and acknowledge nonlinearity, to unveil neural coupling in the sensorimotor system. We highlight recent advances in the field and argue that assessing directionality and nonlinearity of neural coupling will break new ground in the study of the control of movement in healthy and neurologically impaired individuals.

Cross-Frequency Coupling in Descending Motor Pathways: Theory and Simulation

“…The n:m coherence is a straightforward extension of the linear coherence used in corticomuscular coherence (Mima and Hallett, 1999) based on high-order statistics (Nikias and Mendel, 1993) for distinguishably determining cross-and iso-frequency coupling between signals. Thus, the iso-frequency coupling of our results obtained by this method would be comparable to previous corticomuscular coherence studies (Mima and Hallett, 1999;Mima et al, 2001;Yang et al, 2016aYang et al, , 2018.…”

“…The mechanism underlying the changes in IFC and CFC could be associated with the information distortion that occurs across neuron layers leading to decorrelation of the supraspinal input and the motoneuron pool output (Negro and Farina, 2011a). Such distortion is likely caused by the modulation of inter-spike intervals when the motor command is passing through multiple synaptic layers (Koch and Segev, 2000;Markram, 2003;Yang et al, 2018). This modulation could be attributed to (1) heterogeneous recruitment thresholds and spike after-hyperpolarizations of the individual neurons which results in different firing rates for the same steady-state drive (Powers FIGURE 7 | IFC,CFC,and COI between the supraspinal input and cumulative spike train output of the terminal motoneuron pool for the simulated dual input system.…”

“…Neuronal processing of synaptic inputs can lead to the modulation of inter-spike intervals which produces cross-frequency coupling, i.e., synchronization across different frequencies between input and output (Koch and Segev, 2000;Markram, 2003;Yang et al, 2018). Our previous work on multisynaptic ascending sensory pathways (Yang et al, 2016b;Tian et al, 2018), as well as a recent opinion article (Yang et al, 2018), argued that multi-synaptic interaction in a neural pathway can lead to a substantial expression of cross-frequency coupling. However, insights into possible mechanisms underlying neural coupling in the multi-synaptic descending motor pathways are currently lacking.…”

Orchestration of brain oscillations: principles and functions

“…This theme is echoed in the work of Yang et al . () who discuss cross‐frequency coupling during sensorimotor operations, emphasizing that an assumption of linear coupling between systems is not sufficient, and the need for advanced signal‐processing approaches that allow for nonlinearity and provide ways to assess the directionality of such nonlinear coupling (be it ascending or descending).…”

Quantifying the Nonlinear Interaction in the Nervous System Based on Phase-Locked Amplitude Relationship

“…For example, a recent study reported that over 80% of the cortical response to a periodic mechanical stimulus to the wrist joint is caused by nonlinear behavior of the somatosensory system [3]. Thus, assessing nonlinear relations between the stimulus and cortical response may improve our understanding of the communications in the nervous system and could lead to an increased insight of normal and pathological functions [4][5][6].…”