• Abdulrahman Raslan, Philipp Ernst, Marlen Werle, Heike Thieme, Katja Szameit, Mira Finkensieper, Orlando Guntinas-Lichius, and Andrey Irintchev.
• Department of Otorhinolaryngology, University Hospital Jena, Lessingstrasse 2, 07740, Jena, Germany.
• Brain Struct Funct. 2014 May 1; 219 (3): 891-909.

AbstractDeafferentation of motoneurons after facial nerve injury is a well-documented phenomenon but whether synaptic inputs to facial motoneurons are completely restored after reinnervation is unknown. Here, we tested the hypothesis that deficits in motor performance after transection/suture of the facial nerve (facial-facial anastomosis, FFA) in adult rats are associated with incomplete recovery of synaptic inputs. At 2 months after FFA, we found, in congruence with previous results, that the amplitude of whisking had recovered to only 31 % of control (sham operation). In the same FFA-treated rats, estimates of number of chemically defined synaptic terminals in the facial nucleus by immunohistochemistry and stereology showed a significant loss, compared with sham controls, of glutamatergic terminals (-26 %) and cholinergic perisomatic boutons (-31 %), but not inhibitory (GABA/glycinergic) terminals (-14 %). Synaptic deficits were accompanied by persistent microgliosis in the facial nucleus but soma area, dendritic arbor volume, and total number of motoneurons were normal. Correlation analyses revealed significant co-variations of whisking amplitude with number of glutamatergic and cholinergic synapses. Compared with 2 months, analyses of animals at 4 months after FFA showed no attenuation of the functional deficit and structural aberrations with one exception, increase of inhibitory terminal numbers beyond control level (+11 %) leading to further reduction of the excitatory/inhibitory terminal ratio. We suggest that deficits in motoneuron innervation in the regenerated facial nucleus-reduced glutamatergic and cholinergic input and reduced excitatory/inhibitory terminal ratio-could attenuate the motor output and, thus, negatively impact the functional performance after facial nerve regeneration.

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