Abstract
The effects of stimulation of low-threshold proprioceptive afferents in the tibial nerve on two types of excitatory inputs to α-motoneurons were tested. The first input is formed by glutamatergic Ia sensory afferents contacting monosynaptically α-motoneurons. The second one is the cholinergic input originating from V0c—interneurons, located in lamina X of the spinal cord, modulating activity of α-motoneurons via C-terminals. Our aim was to clarify whether enhancement of signaling to ankle extensor α-motoneurons, via direct electrical stimulation addressed predominantly to low-threshold proprioceptive fibers in the tibial nerve of awake rats, will affect Ia glutamatergic and cholinergic innervation of α-motoneurons of lateral gastrocnemius (LG). LG motoneurons were identified with True Blue tracer injected intramuscularly. Tibial nerve was stimulated for 7 days with continuous bursts of three pulses applied in four 20 min sessions daily. The Hoffmann reflex and motor responses recorded from the soleus muscle, LG synergist, allowed controlling stimulation. Ia terminals and C-terminals abutting on LG-labeled α-motoneurons were detected by immunofluorescence (IF) using input-specific anti- VGLUT1 and anti-VAChT antibodies, respectively. Quantitative analysis of confocal images revealed that the number of VGLUT1 IF and VAChT IF terminals contacting the soma of LG α-motoneurons increased after stimulation by 35% and by 26%, respectively, comparing to the sham-stimulated side. The aggregate volume of VGLUT1 IF and VAChT IF terminals increased by 35% and by 30%, respectively. Labeling intensity of boutons was also increased, suggesting an increase of signaling to LG α-motoneurons after stimulation. To conclude, one week of continuous burst stimulation of proprioceptive input to LG α-motoneurons is effective in enrichment of their direct glutamatergic but also indirect cholinergic inputs. The effectiveness of such and longer stimulation in models of injury is a prerequisite to propose it as a therapeutic method to improve inputs to selected group of α-motoneurons after damage.
Highlights
There is an accumulation of the experimental data indicating therapeutic potential of modulation of proprioceptive input to α-motoneurons (MNs) by means of electrical stimulation of low-threshold muscle afferents in peripheral nerves
The electrophysiological data obtained from the animals, which were used in this study, were analyzed and described in our previous article [10]
M1 response and H3 reflex were analyzed as they were not “contaminated” by accompanying M or H responses recruited after 2nd and shortly after 3rd stimulus
Summary
There is an accumulation of the experimental data indicating therapeutic potential of modulation of proprioceptive input to α-motoneurons (MNs) by means of electrical stimulation of low-threshold muscle afferents in peripheral nerves. When combined with operant conditioning this method allows teaching animals to increase an amplitude of H-reflex of ankle extensor MNs, as shown by Wolpaw’s group (reviewed by Chen and co-authors [1]). In trained animals, an increase of H-reflex was found to be persistent and the effect was observed up to 100 days after termination of the operant conditioning [3]. These observations point to profound plasticity of the spinal cord induced by proprioceptive stimulation. Studies aiming to disclose synaptic changes in α-MNs of triceps surae (TS) resulting from the operant conditioning, which lead to an increase of the Hreflexes in the monkey TS muscles, did not bring conclusive results [4] and mechanisms of these changes have not been fully elucidated
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