Contribution of neural circuits tested by transcranial magnetic stimulation in corticomotor control of low back muscle: a systematic review

Abstract

Introduction: Transcranial magnetic stimulation (TMS) is widely used to investigate central nervous system mechanisms underlying motor control. Despite thousands of TMS studies on neurophysiological underpinnings of corticomotor control, a large majority of studies have focused on distal muscles, and little is known about axial muscles (e.g., low back muscles). Yet, differences between corticomotor control of low back and distal muscles (e.g., gross vs. fine motor control) suggest differences in the neural circuits involved. This systematic review of the literature aims at detailing the organisation and neural circuitry underlying corticomotor control of low back muscles tested with TMS in healthy humans.

Methods: The literature search was performed in four databases (CINAHL, Embase, Medline (Ovid) and Web of science) up to May 2022. Included studies had to use TMS in combination with EMG recording of paraspinal muscles (between T12 and L5) in healthy participants. Weighted average was used to synthesise quantitative study results.

Results: Forty-four articles met the selection criteria. TMS studies of low back muscles provided consistent evidence of contralateral and ipsilateral motor evoked potentials (with longer ipsilateral latencies) as well as of short intracortical inhibition/facilitation. However, few or no studies using other paired pulse protocols were found (e.g., long intracortical inhibition, interhemispheric inhibition). In addition, no study explored the interaction between different cortical areas using dual TMS coil protocol (e.g., between primary motor cortex and supplementary motor area).

Discussion: Corticomotor control of low back muscles are distinct from hand muscles. Our main findings suggest: (i) bilateral projections from each single primary motor cortex, for which contralateral and ipsilateral tracts are probably of different nature (contra: monosynaptic; ipsi: oligo/polysynaptic) and (ii) the presence of intracortical inhibitory and excitatory circuits in M1 influencing the excitability of the contralateral corticospinal cells projecting to low back muscles. Understanding of these mechanisms are important for improving the understanding of neuromuscular function of low back muscles and to improve the management of clinical populations (e.g., low back pain, stroke).

Keywords: corticospinal; low back muscle; neural circuits; paired pulse; transcranial magnetic stimulation.

Figure 1

PRISMA flow chart of the systematic review.

Figure 2

Circos plot linking the included studies to their methodological choices. EMG, electromyography; hdEMG, high density electromyography; IHI, interhemispheric inhibition; intra, intramuscular; ICF, intracortical facilitation; MEP, motor evoked potential; MSO, maximum stimulator output; SICF, short intracortical facilitation; SICI, short intracortical inhibition; SP, silent period.

Figure 3

Schematic representation of motor cortex circuits of low back muscles and possible preferential site activation using directional TMS. This model is inspired by Di Lazzaro and Rothwell (2014), Fong et al. (2021), Ziemann (2020). Layers 2 (L2) and 3 (L3) contains interneurons projecting to the pyramidal neurons apical dendrites and layer 5 (L5) includes pyramidal neurons. Two circuits are proposed for PA-TMS late I-wave and AP-TMS delayed late I-wave. GABAergic neurons recruited by SICI paradigms are suggested to connect to corresponding circuit. It remains unclear if different TMS directions recruit different GABAergic SICI circuits. SICF originates through direct excitation (second stimulus) of the axon of interneurons of the late I-wave pathway, which were made hyper excitable by the first stimulus and is a non-synaptic mechanism. Open circles indicate excitatory neurons; Filled circles indicate inhibitory neurons. TMS, transcranial magnetic stimulation; PA, posteroanterior, AP, anteroposterior SICI, short interval intracortical inhibition.

Figure 4

Summary of potential inter-regional influences on M1 for low back muscles. This model is inspired by Reis et al., (2008); Takakusaki (2017). Bold lines from PM, SMA and CBL toward M1: PM, SMA and CBL are known to influence M1 during motor preparation and execution in limb muscles, similar mechanisms may be at play in low back muscles control. Bold lines from M1 toward BS: M1 is usually known as the centre of movement execution, pyramidal cells in M1 are the origin of the descending corticospinal tract. Bold lines between BS and Motoneurons: The pyramidal tract crosses the midline at the level of the BS to reach the muscle contralateral to the stimulated hemisphere. Ipsilateral MEP in low back muscles suggest an ipsilateral tract from one hemisphere to the corresponding ipsilateral muscle. The ipsilateral tract does not cross in the BS. Dashed line from SMA toward BS: SMA has been suggested to be involved in execution of postural command and the strong bilateral projections observed in non-human primates suggest a projection toward motoneurons. Dashed line between both M1s: Interhemispheric influence is suggested between both M1 for low back muscle. BS, brainstem; CBL, cerebellum; M1, primary motor cortex; MEP, motor evoked potential; PM, premotor; SMA, supplementary motor area.