Termination of trigeminal primary afferents on glossopharyngeal–vagal motoneurons: Possible neural networks underlying the swallowing phase and visceromotor responses of prey-catching behavior

Kecskes, Szilvia; Matesz, Clara; Birinyi, András

doi:10.1016/j.brainresbull.2013.09.006

Cited by 5 publications

(5 citation statements)

References 43 publications

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“…Equivalently in frogs, Kecskes et al . discovered that axon collaterals from the spinal- and mesencephalic tract of the trigeminal nerve could be followed into the glossopharyngeal-vagal motor neurons, alongside the perikaryia and dendrites of the nucleus ambiguus (Amb) 20 .…”

Section: Introductionmentioning

confidence: 99%

Visualizing the trigeminovagal complex in the human medulla by combining ex-vivo ultra-high resolution structural MRI and polarized light imaging microscopy

Henssen

Derks

Doorn

et al. 2019

Sci Rep

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A trigeminovagal complex, as described in some animals, could help to explain the effect of vagus nerve stimulation as a treatment for headache disorders. However, the existence of a trigeminovagal complex in humans remains unclear. This study, therefore investigated the existence of the trigeminovagal complex in humans. One post-mortem human brainstem was scanned at 11.7T to obtain structural (T1-weighted) and diffusion magnetic resonance images ((d)MR images). Post-processing of dMRI data provided track density imaging (TDI) maps to investigate white matter at a smaller resolution than the imaging resolution. To evaluate the reconstructed tracts, the MR-scanned brainstem and three additional brainstems were sectioned for polarized light imaging (PLI) microscopy. T1-weighted images showed hyperintense vagus medullar striae, coursing towards the dorsomedial aspect of the medulla. dMRI-, TDI- and PLI-images showed these striae to intersect the trigeminal spinal tract ( sp5 ) in the lateral medulla. In addition, PLI images showed that a minority of vagus fibers separated from the vagus trajectory and joined the trigeminal spinal nucleus (Sp5) and the sp5 . The course of the vagus tract in the rostral medulla was demonstrated in this study. This study shows that the trigeminal- and vagus systems interconnect anatomically at the level of the rostral medulla where the vagus fibers intersect with the Sp5 and sp5 . Physiological and clinical utility of this newly identified interconnection is a topic for further research.

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Section: Introductionmentioning

confidence: 99%

Visualizing the trigeminovagal complex in the human medulla by combining ex-vivo ultra-high resolution structural MRI and polarized light imaging microscopy

Henssen

Derks

Doorn

et al. 2019

Sci Rep

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“…5 summarizes the present and previous data concerning the direct and indirect sensory input to the brainstem networks of preycatching behavior in the frog (Anderson, 2001;Antal et al, 1980;Corbacho et al, 2005;Deak et al, 2009;Harwood and Anderson, 2000;Kecskes et al, 2013Kecskes et al, , 2015Mandal and Anderson, 2010;Matesz, 1994;Matesz et al, 2008Matesz et al, , 2014Nishikawa, 2000). We can hypothesize that direct contacts of the trigeminal fibers with the trigeminal and facial motoneurons can be the morphological background of the synchronization and timing of the jaw closing and opening during the feeding movements.…”

Section: Resultsmentioning

confidence: 85%

“…Several studies (Anderson, 2001;Corbacho et al, 2005;Mandal and Anderson, 2010;Matsushima et al, 1986;Nishikawa, 2000) suggested polysynaptic pathways between sensory fibers and motoneurons involved in the prey catching behavior. Although the possible influence of the primary afferents on the activity of jaw opening muscle is not yet determined, direct contacts have been verified between sensory fibers and various motoneurons supplying jaw closing and tongue muscles as well as those involved in swallowing (Deak et al, 2009;Kecskes et al, 2013Kecskes et al, , 2015Matesz et al, 2008). The jaw opening is executed by the contraction of depressor mandibulae muscle (DMm) under the control of the facial nerve (Gans and Gorniak, 1982;Gaupp, 1904).…”

Section: Introductionmentioning

confidence: 99%

Possible neural network mediating jaw opening during prey-catching behavior of the frog

Kovalecz

Kecskes

Birinyi

et al. 2015

Brain Research Bulletin

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Please cite this article in press as: Kovalecz, G., et al., Termination of trigeminal afferent fibers on facial motoneurons: Possible neural network mediating jaw opening during prey-catching behavior of the frog. Brain Res. Bull. (2015) a b s t r a c tThe prey-catching behavior of the frog is a complex, well-timed sequence of stimulus response chain of movements. After visual analysis of the prey, a size dependent program is selected in the motor pattern generator of the brainstem. Besides this predetermined feeding program, various direct and indirect sensory inputs provide flexible adjustment for the optimal contraction of the executive muscles. The aim of the present study was to investigate whether trigeminal primary afferents establish direct contacts with the jaw opening motoneurons innervated by the facial nerve. The experiments were carried out on Rana esculenta (Pelophylax esculentus), where the trigeminal and facial nerves were labeled simultaneously with different fluorescent dyes. Using a confocal laser scanning microscope, close appositions were detected between trigeminal afferent fibers and somatodendritic components of the facial motoneurons.Quantitative analysis revealed that the majority of close contacts were encountered on the dendrites of facial motoneurons and approximately 10% of them were located on the perikarya. We suggest that the identified contacts between the trigeminal afferents and facial motoneurons presented here may be one of the morphological substrate in the feedback and feedforward modulation of the rapidly changing activity of the jaw opening muscle during the prey-catching behavior.

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“…The trigeminal and vagus nerves perform a central role regarding the interaction between swallowing and cardiac autonomic control. Both nerves are linked to the innervation of the larynx and heart muscles 27 . A study conducted by Kecskes et al 27 employed a confocal laser scanning microscope and investigated brainstem areas involved with the parasympathetic activity and the swallowing phase.…”

Section: Discussionmentioning

confidence: 99%

“…Both nerves are linked to the innervation of the larynx and heart muscles 27 . A study conducted by Kecskes et al 27 employed a confocal laser scanning microscope and investigated brainstem areas involved with the parasympathetic activity and the swallowing phase. These authors advise that motor neurons of nucleus ambiguus and trigeminal afferent terminals are linked for the coordination of muscles related to swallowing phase.…”

Section: Discussionmentioning

confidence: 99%

Effects of effortful swallowing on cardiac autonomic control in individuals with neurogenic dysphagia: a prospective observational analytical study

Silva

Pedroni

et al. 2020

Sci Rep

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Considering that neurogenic oropharyngeal dysphagia is a prevalent condition with or without cardiac disease we should contemplate issues surrounding cardiovascular difficulties during rehabilitation. This study aims to evaluate the effects of effortful swallowing maneuver (ESM) on heart rate variability (HRV) in subjects with neurogenic oropharyngeal dysphagia. We studied 22 individuals [8 Stroke and 14 Parkinson Disease (PD) subjects aged between 41 and 75 years old] with neurogenic oropharyngeal dysphagia regardless of gender. HRV was assessed under two circumstances: spontaneous swallowing versus ESM. Surface electromyography of the suprahyoid muscles was undertaken to measure the swallowing muscle excitation, which then confirmed higher muscle activity during ESM. We attained no changes in HRV between the two swallowing events [HR: spontaneous swallowing 78.68 ± 13.91 bpm vs. ESM 102.57 ± 107.81 bpm, p = 0.201; RMSSD (root-mean square of differences between adjacent normal RR intervals in a time interval): spontaneous swallowing 16.99 ± 15.65 ms vs. ESM 44.74 ± 138.85 ms, p = 0.312; HF (high frequency): spontaneous swallowing 119.35 ± 273 ms 2 vs. ESM 99.83 ± 194.58 ms 2 , p = 0.301; SD1 (standard deviation of the instantaneous variability of the beat-to-beat heart rate): spontaneous swallowing 12.02 ± 1.07 ms vs. ESM 31.66 ± 98.25 ms, p = 0.301]. The effortful swallowing maneuver did not cause clinically significant changes in autonomic control of HR in this group of subjects with oropharyngeal dysphagia.

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Termination of trigeminal primary afferents on glossopharyngeal–vagal motoneurons: Possible neural networks underlying the swallowing phase and visceromotor responses of prey-catching behavior

Cited by 5 publications

References 43 publications

Visualizing the trigeminovagal complex in the human medulla by combining ex-vivo ultra-high resolution structural MRI and polarized light imaging microscopy

Visualizing the trigeminovagal complex in the human medulla by combining ex-vivo ultra-high resolution structural MRI and polarized light imaging microscopy

Possible neural network mediating jaw opening during prey-catching behavior of the frog

Effects of effortful swallowing on cardiac autonomic control in individuals with neurogenic dysphagia: a prospective observational analytical study

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