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Spatial Analysis of Rat Motoneurons that Regenerate their Axons Following Nerve Transection and Coaptation Demonstrates that Chronic Electrical Muscle Stimulation (EMS) Does Not Prevent Random Reinnervation of Target Muscles
Michael P. Willand, PhD1; Joseph Catapano, MD1; Jasmine Burguet, PhD2; Philippe Andrey, PhD2; Gregory H Borschel, MD1; Tessa Gordon, PhD1
1The Hospital for Sick Children, Toronto, ON, Canada, 2Institut Jean-Pierre Bourgin, Versailles, France
Introduction: Regenerating motor nerves randomly reinnervate target muscles resulting in synkinesis. Previous studies in a canine model of laryngeal nerve injury demonstrated through functional measurements that EMS promoted selective reinnervation of muscles. In this study, we examine directly through retrograde labelling and spatial analysis whether or not EMS increases preferential muscle reinnervation.
Methods: The soleus and lateral gastrocnemius (LG) muscles in rats (n=13) were used as the target muscles. The normal soleus motoneuron pool was labelled unilaterally by intramuscular injection of TB. One week later, the lateral gastrocnemius soleus (LGS) nerve was transected and coapted using one epineurial suture and electrodes were implanted into the muscle for EMS. The soleus muscle in one group of rats was subjected to daily EMS, 12 hrs at 20 Hz (10 sec on, 20 sec off, 400 µs pulse width) followed by 12 hrs of intermittent stimulation (10 sec on, 1 hr off). Two months later, the regenerated soleus nerves were retrogradely labelled with Fluoro-Ruby (FR). The contralateral soleus and LG nerves were labelled to determine the distribution of normal motoneuron pools. Labelled motoneurons were counted, and where possible, spatially normalized models were created to analyze and compare the spatial distributions between groups.
Results: Numbers of double labelled soleus motoneurons (TB and FR) were the same in EMS treated and untreated rats demonstrating that EMS did not promote preferential reinnervation of the muscle. Figure 1 shows a 3D representation of all labelled motoneurons. On the uninjured left side, soleus and LG motoneuron distributions that differed significantly are indicated by the red mesh (LG) and blue mesh (soleus). On the reinnervated right side, areas where 80% of reinnervated soleus motoneurons were located are highlighted by a green mesh (sham EMS) and purple mesh (EMS). The distributions of the reinnervated soleus motoneuron pools on the right side were the same whether or not the muscle was subjected to EMS.
Conclusions: Our spatial analysis of retrogradely labelled motoneurons that regenerate their axons after surgical transection and repair of the LGS nerve demonstrate that the motoneuron pools become intermingled randomly irrespective on whether the soleus muscle was subjected to daily EMS. Our results confirm original findings that reinnervation is random and they demonstrate that EMS does not influence this random reinnervation. Importantly, EMS does not prevent muscles from being reinnervated by regenerating nerves.
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