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Axonal mapping of the motor cranial nerves highlights new aspects of high-precision neuromuscular control
Vlad Tereshenko, MD1; Udo Maierhofer, MD1; Dominik Dotzauer, Medical Student1; Roland Blumer, PhD2; Steffen U. Eisenhardt, MD3; Dario Farina, PhD4; Oskar C Aszmann, MD5
1Medical University of Vienna, Vienna, Austria; 2Systemic Anatomy, Medical University of Vienna, Vienna, Austria; 3Medical Center, University of Freiburg, Freiburg, Germany; 4Imperial College London, London, United Kingdom; 5Division of Plastic and Reconstructive Surgery, Medical University of Vienna, Vienna, Austria

Introduction: Cranial neuromuscular systems are among the most highly-controlled effectors in the human body. Basic behaviors, such as swallowing, oral competence, and respiration, must function reliably early on under the most complex circumstances, such as breastfeeding, but must attain an even higher performance level later in life, enabling human interactions, intimacy, and emotional expression. Despite the well-established innervation pattern, the interplay of afferent feedback and motor control in the cranial motor systems remains poorly explored. Methods: Here, we investigated the neuronal sources responsible for motor control of facial, masticatory, and intrinsic tongue muscles in humans using specific molecular markers (NF, CHAT, TH and MBP) to identify different axon types. Results: Quantification analysis revealed more than 10,000 axons each in the facial and hypoglossal nerves, of which 75% were efferent in nature in both nerves. The rest of the facial nerve’s main trunk axon population (25%) comprised non-myelinated sympathetic axons. In contrast, the hypoglossal and masseteric nerves showed motor, sympathetic and, as expected, a significant portion of proprioceptive axon populations. The facial nerve’s branches revealed a mix of motor, sympathetic and additional afferent axon populations. Conclusion: These findings showed that a higher number of motor neuronal sources, compared to muscles in the upper extremity, and rich sensory feedback from mechanoreceptors play a pivotal role in finely-tuned control of the facial and intrinsic tongue muscles. Proprioceptive feedback in the facial muscles is mediated by the trigeminal-facial interconnections. The sympathetic axonal population may explain involuntary control of the muscle tone in the facial muscles, which is indispensable for human interactions.


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