Reduced cholinergic and glutamatergic synaptic input to regenerated motoneurons after facial nerve repair in rats: potential implications for recovery of motor function

• Published in: Brain Structure and Function Vol. 219; no. 3; pp. 891 - 909
• Main Authors: Raslan, Abdulrahman, Ernst, Philipp, Werle, Marlen, Thieme, Heike, Szameit, Katja, Finkensieper, Mira, Guntinas-Lichius, Orlando, Irintchev, Andrey
• Format: Journal Article
• Language: English
• Published: Berlin/Heidelberg Springer Berlin Heidelberg 01-05-2014; Springer Nature B.V
• Subjects: Anatomy & physiology; Animals; Biomedical and Life Sciences; Biomedicine; Cell Biology; Face; Face - innervation; Facial Nerve - surgery; Facial Nerve Injuries - physiopathology; Male; Motor ability; Motor Neurons - physiology; Nerve Regeneration - physiology; Nervous system; Neurology; Neurosciences; Original Article; Presynaptic Terminals - physiology; Rats, Wistar; Recovery of Function - physiology; Rodents; Synapses - physiology; Cholinergic synapses; Stereology; Synaptic terminals; Whisking; Vesicular glutamate transporter 2; Vesicular GABA transporter
• ISSN: 1863-2653; 1863-2661; 0340-2061
• DOI: 10.1007/s00429-013-0542-6

Deafferentation 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.