Newly identified axon types of the facial nerve unveil supplemental neural pathways in the innervation of the face

Tereshenko, Vlad; Maierhofer, Udo; Dotzauer, Dominik C.; Laengle, Gregor; Schmoll, Martin; Festin, Christopher; Luft, Matthias; Rojas, Genova Carrero; Politikou, Olga; Hruby, Laura A.; Klein, Holger Jan; Eisenhardt, Steffen U.; Farina, Dario; Blumer, Roland; Bergmeister, Konstantin D.

doi:10.1016/j.jare.2022.04.009

Cited by 9 publications

(13 citation statements)

References 61 publications

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“…Sympathetic nerve fibers were identified by anti-TH antibodies. Despite the fact that anti-TH specificity has been shown to extend beyond sympathetic nature of the neuronal entities (Brumovsky, 2016;Vyas et al, 2017;Tang and Pierchala, 2022), authors confirmed the neural origin of the sympathetic nerve fibers of the facial nerve in the superior cervical ganglion in a previous study (Tereshenko et al, 2023a). The myelinated fibers were specifically visualized by anti-MBP.…”

Section: Immunofluorescence Labelingmentioning

confidence: 74%

“…Therefore, it has been historically accepted that control of the facial muscles is provided solely by motor neuronal input of the facial nerve and controversies regarding the nature of neural feedback from the facial muscles have emerged over the past years (Carmichael and Woollard, 1933;Cobo et al, 2017). The view of a purely motor facial nerve has been questioned in a recent experimental study (Tereshenko et al, 2023a) but the extent of non-motor axons in facial muscle control remains unclear yet.…”

Section: Introductionmentioning

confidence: 99%

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Axonal mapping of the motor cranial nerves

et al. 2023

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Basic behaviors, such as swallowing, speech, and emotional expressions are the result of a highly coordinated interplay between multiple muscles of the head. Control mechanisms of such highly tuned movements remain poorly understood. Here, we investigated the neural components responsible for motor control of the facial, masticatory, and tongue muscles in humans using specific molecular markers (ChAT, MBP, NF, TH). Our findings showed that a higher number of motor axonal population is responsible for facial expressions and tongue movements, compared to muscles in the upper extremity. Sensory axons appear to be responsible for neural feedback from cutaneous mechanoreceptors to control the movement of facial muscles and the tongue. The newly discovered sympathetic axonal population in the facial nerve is hypothesized to be responsible for involuntary control of the muscle tone. These findings shed light on the pivotal role of high efferent input and rich somatosensory feedback in neuromuscular control of finely adjusted cranial systems.

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Section: Immunofluorescence Labelingmentioning

confidence: 74%

Section: Introductionmentioning

confidence: 99%

Axonal mapping of the motor cranial nerves

et al. 2023

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“…However, smooth muscles (targeted by the parasympathetic system) and skeletal muscles (targeted by the somatic efferent system) differ in their ultrastructural morphology, physiology, and embryogenesis (Waite and Li, 1993;Somlyo and Somlyo, 1994;Eddinger, 1998). A previous study reported on the sympathetic axons in the extracranial facial nerve, which highlighted their possible contribution to the maintenance and modulation of neuromuscular junctions (Takeuchi et al, 1993;Tereshenko et al, 2022). One of the intriguing questions is whether the neural input is essential for differentiated properties of the muscle tissue and if it can determine not only the different transcriptome activations but remodel morphologic and physiologic properties of muscle tissue as well (de Medinaceli and Rawlings, 1987;Weng et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Autonomic Nerve Fibers Aberrantly Reinnervate Denervated Facial Muscles and Alter Muscle Fiber Population

Luft

Dotzauer²,

Ortmayr³

et al. 2022

J. Neurosci.

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The surgical redirection of efferent neural input to a denervated muscle via a nerve transfer can reestablish neuromuscular control after nerve injuries. The role of autonomic nerve fibers during the process of muscular reinnervation remains largely unknown. Here, we investigated the neurobiological mechanisms behind the spontaneous functional recovery of denervated facial muscles in male rodents. Recovered facial muscles demonstrated an abundance of cholinergic axonal endings establishing functional neuromuscular junctions. The parasympathetic source of the neuronal input was confirmed to be in the pterygopalatine ganglion. Furthermore, the autonomically reinnervated facial muscles underwent a muscle fiber change to a purely intermediate muscle fiber population myosin heavy chain type IIa. Finally, electrophysiological tests revealed that the postganglionic parasympathetic fibers travel to the facial muscles via the sensory infraorbital nerve. Our findings demonstrated expanded neuromuscular plasticity of denervated striated muscles enabling functional recovery via alien autonomic fibers. These findings may further explain the underlying mechanisms of sensory protection implemented to prevent atrophy of a denervated muscle.SIGNIFICANCE STATEMENTNerve injuries represent significant morbidity and disability for patients. Rewiring motor nerve fibers to other target muscles has shown to be a successful approach in the restoration of motor function. This demonstrates the remarkable capacity of the CNS to adapt to the needs of the neuromuscular system. Yet, the capability of skeletal muscles being reinnervated by nonmotor axons remains largely unknown. Here, we show that under deprivation of original efferent input, the neuromuscular system can undergo functional and morphologic remodeling via autonomic nerve fibers. This may explain neurobiological mechanisms of the sensory protection phenomenon, which is because of parasympathetic reinnervation.

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“…The generalized stratification of nerves into sensory or motor types does not accurately reflect the true axonal architecture of a particular nerve, as neither motor nor sensory nerves contain exclusively efferent or afferent nerve fibers. 2,3 Even those motor branches that innervate the neuromuscular junctions within the muscle must contain Ia afferent proprioceptive nerve fibers, given that motor control of almost all skeletal muscles relies on proprioceptive feedback. 4…”

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confidence: 99%

“…However, the origin of the Tinel sign along these grafts has remained unclear because of the traditional view of the extracranial facial nerve as a pure motor nerve. 3 Recent findings have highlighted an afferent axonal population of facial nerve branches that originates from trigeminal nerve fibers. 3 Thus, a positive Tinel sign only resonates axonal regeneration of the sensory axons traveling through the cross-face nerve graft from the trigeminal nerve fibers that do not contribute to motor restoration of facial expressions (Fig.…”

mentioning

confidence: 99%

Beyond the tingling sensation: unveiling the neurobiological origin of the Hoffmann-Tinel sign

Tereshenko,

Aszmann,

Eberlin

et al. 2023

Plastic &Amp; Reconstructive Surgery

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Volume 153, Number 4 • Viewpoints 857e visuals help in clarifying the treatment process and causal relationship upon medical disputes. We believe that, as in Feynman diagrams, these aesthetic diagrams have the potential to promote positive combined therapies, prevent negative outcomes, and become a highly valued tool for complex recording, documentation, and presentation in daily aesthetic practice.

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Newly identified axon types of the facial nerve unveil supplemental neural pathways in the innervation of the face

Cited by 9 publications

References 61 publications

Axonal mapping of the motor cranial nerves

Axonal mapping of the motor cranial nerves

Autonomic Nerve Fibers Aberrantly Reinnervate Denervated Facial Muscles and Alter Muscle Fiber Population

Beyond the tingling sensation: unveiling the neurobiological origin of the Hoffmann-Tinel sign

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