Abstract
Coupling of neural oscillations is essential for the transmission of cortical motor commands to motoneuron pools through direct and indirect descending motor pathways. Most studies focus on iso-frequency coupling between brain and muscle activities, i.e., cortico-muscular coherence, which is thought to reflect motor command transmission in the mono-synaptic corticospinal pathway. Compared to this direct pathway, indirect corticobulbospinal motor pathways involve multiple intermediate synaptic connections via spinal interneurons. Neuronal processing of synaptic inputs can lead to modulation of inter-spike intervals which produces cross-frequency coupling. This theoretical study aims to evaluate the effect of the number of synaptic layers in descending pathways on the expression of cross-frequency coupling between supraspinal input and the cumulative output of the motoneuron pool using a computer simulation. We simulated descending pathways as various layers of interneurons with a terminal motoneuron pool using Hogdkin–Huxley styled neuron models. Both cross- and iso-frequency coupling between the supraspinal input and the motorneuron pool output were computed using a novel generalized coherence measure, i.e., n:m coherence. We found that the iso-frequency coupling is only dominant in the mono-synaptic corticospinal tract, while the cross-frequency coupling is dominant in multi-synaptic indirect motor pathways. Furthermore, simulations incorporating both mono-synaptic direct and multi-synaptic indirect descending pathways showed that increased reliance on a multi-synaptic indirect pathway over a mono-synaptic direct pathway enhances the dominance of cross-frequency coupling between the supraspinal input and the motorneuron pool output. These results provide the theoretical basis for future human subject study quantitatively assessing motor command transmission in indirect vs. direct pathways and its changes after neurological disorders such as unilateral brain injury.
Highlights
The human motor system is a highly cooperative network comprised of different groups of neurons
Neural Coupling Between the Supraspinal Input and the Cumulative Output From Motoneuron Pool. Both iso-frequency coupling and cross-frequency coupling were detected in the simulated motor pathways
To examine how iso-frequency coupling and cross-frequency coupling evolved with increasing interneuron layers, we computed the IFC, CFC, and COI between the given supraspinal input and the motoneuron pool output for simulated pathways with various layers (N = 0, 1, 2, 3, . . . ) of interneurons in cascade with a terminal motoneuron pool
Summary
The human motor system is a highly cooperative network comprised of different groups of neurons. Previous simulation and in vivo studies demonstrated that, in this direct descending pathway, despite the non-linearity of individual neurons, neural oscillation of the supraspinal input could be linearly transmitted to the cumulative output of the motoneuron pool at the same frequency (Negro and Farina, 2011a,b). These previous studies explained the origin of iso-frequency coupling between the supraspinal input and the motoneuron pool output with respect to the use of the monosynaptic corticospinal tract as the fastest, direct descending pathways in healthy individuals
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