Original Articles
Long-term observation on the changes of somatotopy in the facial nucleus after nerve suture in the cat: Morphological studies using retrograde labeling

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Abstract

To examine the time course of plasticity of the cranial nucleus during axonal regeneration, we followed the topographical reorganization of the cat facial nucleus (FN) up to 24 months after facio-facial nerve suture using retrograde labeling methods. The trunk of the temporal-zygomatico-orbital and both superior and inferior buccolabial branches (defined as main branch) of the facial nerve was cut and sutured again under ketamine hydrochloride anesthesia. At 11–722 days after nerve suture, Fast Blue (FB) and 1,1′-dioctadecyl-3, 3, 3′, 3′-tetramethylindocarbocyanine perchlorate (DiI) or horseradish peroxidase (HRP) were injected into the distal part of the sutured main branch and the unoperated posterior auricular branch, respectively. Until about 3 months after suture, the topographical pattern in FN was similar to that observed in normal cats. At about 4 months after suture, FB-labeled motoneurons were distributed not only in the lateral part (including intermediate, dorsal and ventrolateral divisions) but also in the medial subdivision of FN. After a survival period of 18–24 months, FB-labeled neurons were found all over the FN, and their number increased significantly. Interestingly, in the longer survival cases, we noticed that the DiI- or HRP-labeled posterior auricular branch motoneurons also showed a tendency to distribute outside the medial region. The present study showed that somatotopic disorganization starts at around 4 months after suture, which seems to be somewhat slower than that in rats, and continues until a much later postoperative period. Furthermore, we suggested a possibility that the regeneration of one branch may affect the somatotopy of the unoperated nerve branch. These phenomena may contribute to aberrant facial nerve functions such as abnormal associated movement and facial spasm observed after nerve injury.

Introduction

It is well confirmed that peripheral nerves can regenerate after nerve injury, and recovery of motor function following damage is due to the ability of motor nerves to sprout and reinnervate denervated peripheral targets 7, 8, 10, 18, 25, 27. Studies on the nerve suture have been done in the spinal nerve, and they have shown that plastic changes occur in the sensory and motor system in the spinal cord, that is, changes of distribution of sensory terminals, hyperinnervation to target muscles or reorganization of the motor neuron pool 1, 6, 10, 24, 29.

In the cranial nerves, facial and hypoglossal nerves have been extensively studied, because these nerves are mostly composed of motor axons and the functional recovery from facial palsy has a clinical importance 2, 3, 9, 12, 21, 23, 26, 28, 30. Although there might be some controversy on the survival of cranial motor neurons after nerve transection [5], it seemed to be clear that cranial nerve suture also brought similar plastic changes to those reported in the spinal cord. For example, Mizuno et al. [20] reported that somatotopic reorganization in the hypoglossal nucleus was observed 4–6 months after suture in the cat. After facio-facial or hypoglossal-facial nerve suture, Angelov et al. reported hyperinnervation to the facial muscles as well as somatotopic disorganization 3, 4. However, most of these previous studies have examined the effects of neural regeneration at 3–4 weeks or within 1 year after operation 2, 3, 4, 9, 11, 13, 14, 20, 22, 26, 28, 30, and little is known about the features of neural reorganization in the cat facial nucleus (FN) during a long period after nerve suture.

In the present study, we first examined the time course of the facial nerve regeneration and the topographical reorganization of FN using retrograde labeling methods. We report that functional regeneration occurred rather early after suture and that changes of the topographical organization in FN started at much longer postoperative times. The present study indicates that nerve regeneration seems to be important to bring the topographical reorganization of the neuron pool and may cause some interaction between FN subnuclei.

Section snippets

Materials and methods

The present study was performed on 29 cats (8 were normal, 19 were sutured and 2 were axotomized). Under ketamine hydrochloride anesthesia (20 mg/kg, i.m.), the trunk of the temporal-zygomatico-orbital and both superior and inferior buccolabial branches—main branch (MB)—was cut by scissors, then immediately sutured again with a 9-0 nylon thread under an operating microscope. In axotomized cats, proximal cut ends were tightly ligated. The disappearance of the blink reflex was confirmed after the

Results

In the present study, we examined the blink reflex as a functional recovery of facial nerve-muscle connection. The blink reflex usually reappeared at the beginning of the third postoperative week. However, we did not examine it systematically and will show the morphological data in the following sections. For the morphological study, we attempted to explore the time course of the reorganization of regenerating MB motoneurons.

Discussion

The peripheral nerve reconstruction has a long clinical history, and extensive studies have been done to explore the basic mechanisms of the nerve regeneration and the effects of nerve regeneration on the motor neuron pool 10, 18. In the cranial nerves, functional reconstruction of the facial nerve has been conducted by facio-facial or hypoglossal-facial anastomosis, but the functional recovery in the clinical cases seems to be not so sufficient in some cases, that is, appearance of aberrant

Acknowledgements

We thank Mrs. J. Kobayashi for her excellent technical assistance. This work was partly supported by Grants-in-Aid (1997) from the Mie Medical Research Foundation and from the Ministry of Education, Science and Culture of Japan (0668080).

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