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Quantity and Three-Dimensional Position of the Recurrent and Superior Laryngeal Nerve Lower Motor Neurons in a Rat Model

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Quantity and Three-Dimensional Position of the Recurrent and Superior Laryngeal Nerve Lower Motor Neurons in a Rat Model Annals of Otology. Rhinology & iMryngology 120(ll):761-768. © 2011 Annals Publishing Company. All rights reserved. Quantity and Three-Dimensional Position of the Recurrent and Superior Laryngeal Nerve Lower Motor Neurons in a Rat Model Philip Weissbrod, MD; Michael J. Pitman, MD; Sansar Sharma, MD; Aaron Bender; Steven D. Schaefer, MD Objectives: We sought to elucidate the 3-dimensiotial position and quantify the lower motor neurons (LMNs) of the re- current laryngeal nerve (RLN) and the superior laryngeal nerve (SLN) in a rat model. Quantification and mapping of these neurons will enhance the usefulness of the rat model in the study of reinnervation following trauma to these nerves. Methods: Female Sprague-Dawley rats underwent microsurgical transaction of the RLN, the SLN, or both the RLN and SLN or sham surgery. After transection, either Fluoro-Ruby (FR) or Fluoro-Gold (FG) was applied to the proximal nerve stumps. The brain stems were harvested, sectioned, and examined for fluorolabeling. The LMNs were quantified, and their 3-dimensional position within the nucleus ambiguus was mapped. Results: Labeling of the RLN was consistent regardless of the labeling agent used. A mean of 243 LMNs was document- ed for the RLN. The SLN labeling with FR was consistent and showed a mean of 117 LMNs; however, FG proved to be highly variable in labeling the SLN. The SLN LMNs lie rostral and ventral to those of the RLN. In the sham surgical condition, FG was noted to contaminate adjacent tissues — in particular, in the region of the SLN. Conclusions: Fluorolabeling is an effective tool to locate and quantify the LMNs of the RLN and SLN. The LMN po- sitions and counts were consistent when FR was used in labeling of either the RLN or the SLN. Fluoro-Gold, however, because of its tendency to contaminate surrounding structures, can only be used to label the RLN. Also, as previously reported, the SLN LMNs lie rostral and ventral to those of the RLN. This information results in further clarification of a rat model of RLN injury that may be used to investigate the effects of neurotrophic factors on RLN reinnervation. Key Words: animal model, Fluoro-Gold, Fluoro-Ruby, laryngeal nerve, lower motor neuron. INTRODUCTION cles. Both of these considerations require resolution Iatrogenic injury to the laryngeal nerves is a rel- at the laryngeal muscle and the laryngeal motor neu- atively common complication of thyroid, cervical, ron in the brain stem. An animal model is critical or cardiothoracic surgery. The recurrent laryngeal to understanding the cause of synkinesis and later nerve (RLN) and the superior laryngeal nerve (SLN) devising treatments to potentiate the proper regen- serve as conduits of both motor information and sen- eration of the RLN. Such a model would need to be sory information to and from the larynx. The RLN investigated by endoscopie, electromyographic, and innervates both adductor and abductor muscles in histologie techniques to elucidate the neurologic re- the larynx. After transection of the RLN, the aber- generative processes that occur at both the larynx rant regeneration of the axons results in synkinesis and the lower motor neurons (LMNs) in the nucle- that leads to vocal fold immobility. us ambiguus (NA). In the present study, we aimed to update the rat model by elucidating the 3-dimen- Synkinesis of laryngeal muscles may be consid- sional organization of the LMNs of the RLN and the ered in two ways. In one, a single regenerating RLN SLN. We provide an accurate reference for future axon may innervate both adductor and abductor experiments involving retrograde labeling via mus- muscles. Conversely, regenerating axons may inap- cle injections and direct application of tracers to the propriately innervate the adductor or abductor mus- RLN after injury. These future experiments will en- cle, with abductor axons innervating adductor mus- hance our understanding of the mechanism of synki- cles and adductor axons innervating abductor mus- nesis and exploration of treatment to restore proper From the Department of Otolaryngology, New York Eye and Ear Infirmary, New York (Weissbrod, Pitman, Schaefer), and the Depart- ment of Cell Biology, New York Medical College, Valhalla (Sharma, Bender), New York. This study was pertbrmed in accordance with the PHS Policy on Humane Care and Use of Laboratory Animals, the NIH Guide for the Care and Use of Lahorulory Animals, and the Animal Welfare Act (7 U.S.C. et seq.); the animal use protocol was approved by the Institutional Animal Care and Use Committee (IACUC) of New York Medical College. Presented at the meeting of the American Broncho-Esophagological Association, Las Vegas, Nevada, April 28-29, 2010. Correspondence: Michael J. Pitman, MD, 310 E 14th St. 6th Floor. New York Eye and Ear Infirmary, New York, NY 10003. 761 762 Weissbrod et al. Recurrent & Superior Laryngeal Nerve Lower Motor Neurons function via accurate reinnervation. RLN was labeled with FG and the SLN with FR. In a second group of 4, the RLN was labeled with FR Previous studies have examined the NA in rats and the SLN with FG. In a third group (8 total), 4 by using retrograde labeling with variable results.'-^ animals had only the RLN labeled with FR and the The current study was intended to reexamine the lo- other 4 had only the SLN labeled with FR. Sham cation and quantity of LMNs within the NA, and surgery and labeling was performed on a fourth specifically the relationship between the RLN LMNs group of 4 animals. and the SLN LMNs, through the use of more sophis- ticated labeling agents that enable complete visual- Surgical Procedures. Each animal was sedated ization of neurons, dendrites, and axons. We chose with isoflurane and then received an intramuscu- Fluoro-Ruby (FR; Invitrogen, Carlsbad, California) lar injection of 70 mg/kg of ketamine hydrochloride and Fluoro-Gold (FG; Fluorochrome LLC, Denver, and 7 mg/kg xylazine hydrochloride to produce suf- Colorado) because they are easily processed and al- ficient anesthesia. The anterior cervical region was low for clear visualization of labeled cells. Via retro- injected subcutaneously with 0.2 mL of 1% lido- grade transport, these chemicals avidly label LMNs caine hydrochloride with epinephrine (1:100,000). and their processes in a relatively short period of Anesthesia was confirmed with a tail and foot pinch time and remain in the cell bodies for many months before the surgical procedure commenced. without transsynaptic labeling.'' The animals were placed supine, and a vertical midline incision was made extending to the ster- METHODS num. The strap muscles were separated in the mid- Experimental Animals. Twenty female Sprague line and retracted with an eyelid retractor. With an Dawley rats weighing 250 g were used in the pres- operating microscope (Cari Zeiss AG, Oberkochen, ent study. Humane care was provided for the ani- Germany), the RLN was identified in the tracheo- mals, and all institutional and national guidelines esophageal groove and isolated from its surround- were observed. The animals underwent transection ing structures. The SLN was identified as it coursed of the right RLN only (4 animals), the right SLN horizontally to the cricothyroid muscle. Depending only (4 animals), or both the RLN and SLN (8 ani- on the experimental condition, the RLN, the SLN, mals) or sham surgery (4 animals). After transec- or both the RLN and SLN were sharply transected. tion, the proximal nerve stumps were soaked in la- The RLN was transected at the level of the seventh beling agent consisting of 5% FG in 0.1 mol/L phos- trachéal ring, and the SLN was transected just prox- phate-buffered saline solution (PBS) or 5% FR in imal to its entry into the larynx. After transection, PBS for a period of 5 minutes for retrograde label- fluorochrome was applied to the proximal nerve ing of the neurons in the brain stem. The transected stump for a period of' 5 minutes. In cases in which nerve end was isolated from the surrounding fascia dual labeling was performed, cotton was placed be- and smooth muscles, Gelfoam soaked with the fluo- tween the labeling sites to prevent contamination. In rochrome was then packed around the transected all experiments, only the right RLN and right SLN nerve end and left in place for 5 minutes. After this were transected, with the contralateral side serving procedure, the cut nerve was thoroughly washed as a control. After nerve labeling, the area was blot- with PBS and the area was dried with cotton swabs ted with cotton to remove excess tracer, and the in- to minimize contamination of the dye in the sur- cision was closed with 3-0 silk suture. To confirm rounding tissue. This technique was an alternative injury to the RLN, we performed transoral laryngos- to placing the nerve end in a well filled with tluoro- copy with a 0° rigid nasal endoscope (Karl Storz, chrome. In previous experiments, the well technique Tuttlingen, Germany) to confirm absence of move- appeared to result in more nerve end trauma, as well ment and vocal fold paralysis. as contamination of surrounding tissue. For sham surgical procedures, the above process The choice of these fluorochromes was based was performed, including identification and isola- upon our previous work. Fluoro-Gold may pene- tion of the appropriate nerves. Gelfoam soaked with trate intact axons and label other neurons in the fluorolabeling agent was packed around the uncut brain stem. This situation was avoided by the isola- nerve at the site for a period of 5 minutes. The Gel- tion and washing of the nerve after exposure to the foam was removed, the area was blotted with cotton, fluorochrome. Fluoro-Ruby, on the other hand, has and the wound was closed in the above fashion.
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