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

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

doi:10.1371/journal.pone.0192471

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

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

Department of Clinical Medicine

6 Citations (Scopus)

49 Downloads (Pure)

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.

Original language	English
Article number	e0192471
Journal	PLoS ONE
Volume	13
Issue number	2
Number of pages	13
ISSN	1932-6203
DOIs	https://doi.org/10.1371/journal.pone.0192471
Publication status	Published - Feb 2018

Keywords

Adult
Female
H-Reflex
Humans
Male
Median Nerve/physiology
Middle Aged
Motor Neurons/physiology
Muscle, Skeletal/innervation
Spinal Cord/cytology
Tibial Nerve/physiology
Transcutaneous Electric Nerve Stimulation/methods
Young Adult

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title = "Effects of patterned peripheral nerve stimulation on soleus spinal motor neuron excitability",

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.",

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author = "Samuel Jimenez and Laura Mordillo-Mateos and Michele Dileone and Michela Campolo and Carmen Carrasco-Lopez and Fabricia Moitinho-Ferreira and Tomas Gallego-Izquierdo and Siebner, {Hartwig R} and Josep Valls-Sol{\'e} and Juan Aguilar and Antonio Oliviero",

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doi = "10.1371/journal.pone.0192471",

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T1 - Effects of patterned peripheral nerve stimulation on soleus spinal motor neuron excitability

AU - Jimenez, Samuel

AU - Mordillo-Mateos, Laura

AU - Dileone, Michele

AU - Campolo, Michela

AU - Carrasco-Lopez, Carmen

AU - Moitinho-Ferreira, Fabricia

AU - Gallego-Izquierdo, Tomas

AU - Siebner, Hartwig R

AU - Valls-Solé, Josep

AU - Aguilar, Juan

AU - Oliviero, Antonio

PY - 2018/2

Y1 - 2018/2

N2 - 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.

AB - 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.

KW - Adult

KW - Female

KW - H-Reflex

KW - Humans

KW - Male

KW - Median Nerve/physiology

KW - Middle Aged

KW - Motor Neurons/physiology

KW - Muscle, Skeletal/innervation

KW - Spinal Cord/cytology

KW - Tibial Nerve/physiology

KW - Transcutaneous Electric Nerve Stimulation/methods

KW - Young Adult

U2 - 10.1371/journal.pone.0192471

DO - 10.1371/journal.pone.0192471

M3 - Journal article

C2 - 29451889

SN - 1932-6203

VL - 13

JO - PLoS ONE

JF - PLoS ONE

IS - 2

M1 - e0192471

ER -

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

Abstract

Keywords

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