Research Article: Effects of patterned peripheral nerve stimulation on soleus spinal motor neuron excitability

Date Published: February 16, 2018

Publisher: Public Library of Science

Author(s): Samuel Jimenez, Laura Mordillo-Mateos, Michele Dileone, Michela Campolo, Carmen Carrasco-Lopez, Fabricia Moitinho-Ferreira, Tomas Gallego-Izquierdo, Hartwig R. Siebner, Josep Valls-Solé, Juan Aguilar, Antonio Oliviero, François Tremblay.

http://doi.org/10.1371/journal.pone.0192471

Abstract

Spinal plasticity is thought to contribute to sensorimotor recovery of limb function in several neurological disorders and can be experimentally induced in animals and humans using different stimulation protocols. In healthy individuals, electrical continuous Theta Burst Stimulation (TBS) of the median nerve has been shown to change spinal motoneuron excitability in the cervical spinal cord as indexed by a change in mean H-reflex amplitude in the flexor carpi radialis muscle. It is unknown whether continuous TBS of a peripheral nerve can also shift motoneuron excitability in the lower limb. In 26 healthy subjects, we examined the effects of electrical TBS given to the tibial nerve in the popliteal fossa on the excitability of lumbar spinal motoneurons as measured by H-reflex amplitude of the soleus muscle evoked by tibial nerve stimulation. Continuous TBS was given at 110% of H-reflex threshold intensity and compared to non-patterned regular electrical stimulation at 15 Hz. To disclose any pain-induced effects, we also tested the effects of TBS at individual sensory threshold. Moreover, in a subgroup of subjects we evaluated paired-pulse inhibition of H-reflex. Continuous TBS at 110% of H-reflex threshold intensity induced a short-term reduction of H-reflex amplitude. The other stimulation conditions produced no after effects. Paired-pulse H-reflex inhibition was not modulated by continuous TBS or non-patterned repetitive stimulation at 15 Hz. An effect of pain on the results obtained was discarded, since non-patterned 15 Hz stimulation at 110% HT led to pain scores similar to those induced by EcTBS at 110% HT, but was not able to induce any modulation of the H reflex amplitude. Together, the results provide first time evidence that peripheral continuous TBS induces a short-lasting change in the excitability of spinal motoneurons in lower limb circuitries. Future studies need to investigate how the TBS protocol can be optimized to produce a larger and longer effect on spinal cord physiology and whether this might be a useful intervention in patients with excessive excitability of the spinal motorneurons.

Partial Text

Spinal plasticity can be triggered in animal and human spinal cord using different experimental protocols [1,2] For instance, spinal plasticity can be induced by behavioural manipulation [3], or by repetitive electrical stimulation of the ventral horn of the spinal cord in vitro[4].

Data are reported as mean and standard errors of the mean. Main outcome measures were: 1) H reflex amplitude normalized to the Mmax (H/Mmax); 2) the grand mean of H2/H1 ratio at ISIs of 50ms and 100ms (mean of H2/H150ms and H2/H1100ms) and 3) pain (caused by the interventions at 110%HT). The score obtained from VAS evaluation of stimulus-induced pain was compared among protocols using an unpaired t test. A mixed factorial ANOVA on values normalized to the baseline with factors of TIME (post1/baseline, and post2/baseline) and PROTOCOL (the three GROUPS of subjects submitted to different stimulation conditions: EcTBS110HT and EcTBSST and 15Hz110HT) were used to compare the effects on the H/Mmax ratio between the three different stimulation protocols. TIME was considered as within-subjects factor and PROTOCOL/GROUP was considered as between-subjects factor. Post hoc tests were performed using Tukey Honest. A separate mixed factorial ANOVA on values normalized to the baseline with factors of TIME (post1/baseline, and post2/baseline) and PROTOCOL (the three GROUPS of subjects receiving different intervention: EcTBS110HT and EcTBSST and 15Hz110HT) were used to compare the effects on the H2/H1 ratio between the three different stimulation protocols. Again, TIME was considered as within-subjects factor and PROTOCOL/GROUP was considered as between-subjects factor. Post hoc tests were performed using Tuckey Honest. Differences were considered significant when p<0.05. The subjects that participated in the EcTBSST reported no pain during the protocol. The subjects, that participated in the experiments at 110% HT reported pain sensation to stimulation trains that did not significantly differ between both, EcTBS110HT and 15Hz110HT: (5.9±1.7 and 7±1.2, respectively; p = 0.1029) (Fig 2, panel C). Baseline H-reflex thresholds (EcTBS110HT vs 15Hz110HT, p = 0.268), baseline H-reflex amplitude (EcTBS110HT vs 15Hz110HT, p = 0.757; EcTBS110HT vs EcTBSST, p = 0.327; 15Hz110HT vs EcTBSST, p = 0.124), baseline M wave amplitude (EcTBS110HT vs 15Hz110HT, p = 0.367; EcTBS110HT vs EcTBSST, p = 0.434; 15Hz110HT vs EcTBSST, p = 0.849) and baseline Mmax amplitude (EcTBS110HT vs 15Hz110HT, p = 0.136; EcTBS110HT vs EcTBSST, p = 0.554; 15Hz110HT vs EcTBSST, p = 0.434) were similar in the three protocols (Table 1). Tibial nerve stimulation intensities to obtain a stable H reflex and M wave, in baseline, are reported in Table 1. The intensity used was around 150% HT in EcTBS110HT and 15Hz110HT. In the present study, we show that the application of 40 seconds EcTBS (600 pulses) at 110% of the H-reflex threshold intensity induced a short term reduction of the H/Mmax ratio after the end of the stimulation while EcTBS at ST and 15 Hz non-patterned stimulation did not. None of the stimulation protocols used was able to induce any change in PPI of the H-reflex.   Source: http://doi.org/10.1371/journal.pone.0192471

 

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