Effect of pharmacological inhibition of the pontine respiratory group on swallowing interneurons in the dorsal medulla oblongata

Takemura, Akiyo; Sugiyama, Yoichiro; Yamamoto, Ryota; Kinoshita, Shingo; Kaneko, Mitsuaki; Fuse, Shinya; Hashimoto, Keiko; Mukudai, Shigeyuki; Umezaki, Toshiro; Dutschmann, Mathias; Hirano, Shigeru

doi:10.1016/j.brainres.2022.148101

Cited by 6 publications

(4 citation statements)

References 53 publications

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“…However, when separating out pharyngeal versus laryngeal inputs, sensory-motor coordination during the pharyngeal phase of physiological swallows is more complex (Yamamoto et al, 2022). Effects of pontine respiratory group inhibition on swallow function differed between SLN stimulated swallow and physiological swallows which has been attributed to the sensory feedback of the SPG (Takemura et al, 2022). Though, fictive swallows via SLN stimulation, similar to physiological water-evoked swallows, occur during respiratory phase transitions including late expiration to inspiration and inspiration to postinspiration (Dick, Oku, Romaniuk, & Cherniack, 1993).…”

Section: Discussionmentioning

confidence: 99%

Postinspiratory complex acts as a gating mechanism regulating swallow-breathing coordination and other laryngeal behaviors

Huff¹,

Amarante²,

Oliveira³

et al. 2023

Preprint

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Breathing needs to be tightly coordinated with upper airway behaviors, such as swallowing. Discoordination leads to aspiration pneumonia, the leading cause of death in neurodegenerative diseases. Here we study the role of the postinspiratory complex, (PiCo) in coordinating breathing and swallowing. Using optogenetic approaches in freely breathing-anesthetized ChATcre, Vglut2cre and co-transmission of hATcre/Vglut2FlpO mice reveals this small brainstem microcircuit acts as a central gating mechanism for airway protective behaviors. Activation of PiCo during inspiration or the beginning of postinspiration triggers swallow behavior, while there is a higher probability for stimulating laryngeal activation when activated further into expiration, suggesting PiCo's role in swallow-breathing coordination. PiCo triggers consistent swallow behavior and preserves physiologic swallow motor sequence, while stimulates laryngeal activation variable to stimulation duration. Sufficient bilateral PiCo activation is necessary for gating function since activation of only a few PiCo neurons or unilateral activation leads to blurred behavioral response. Viral tracing experiments reveal projections from the caudal nucleus of the solitary tract (cNTS), the presumed swallow pattern generator (SPG), to PiCo and vice versa. However, PiCo does not directly connect to laryngeal muscles. Investigating PiCo's role in swallow and laryngeal coordination will aid in understanding discoordination in breathing and neurological diseases.

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Section: Discussionmentioning

confidence: 99%

Postinspiratory complex acts as a gating mechanism regulating swallow-breathing coordination and other laryngeal behaviors

Huff¹,

Amarante²,

Oliveira³

et al. 2023

Preprint

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“…Generally, the respiratory cycle can be divided into inspiration, early expiration (also known as post-inspiration), and late expiration phases. Swallow is inhibited during the inspiration phase ( 16 , 17 ). Based on this fact and considering the desirability of the expiration phase for swallow timing, we proposed a method that involves electrical stimulation of sensory nerves which travel through pathways within the spinal cord.…”

Section: Introductionmentioning

confidence: 99%

Stochastic electrical stimulation of the thoracic or cervical regions with surface electrodes facilitates swallow in rats

Kitamura,

Frazure,

Iceman

et al. 2024

Front. Neurol.

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IntroductionAspiration pneumonia, a leading cause of mortality, poses an urgent challenge in contemporary society. Neuromuscular electrical stimulation (NMES) has been commonly used in dysphagia rehabilitation. However, given that NMES at motor threshold targets only specific muscles, it carries a potential risk of further compromising functions related to swallowing, respiration, and airway protection. Considering that the swallow motor pattern is orchestrated by the entire swallow pattern generator (the neural mechanism governing a sequence of swallow actions), a rehabilitation approach that centrally facilitates the entire circuit through sensory nerve stimulation is desirable. In this context, we propose a novel stimulation method using surface electrodes placed on the back to promote swallowing.MethodsThe efficacy of the proposed method in promoting swallowing was evaluated by electrically stimulating sensory nerves in the back or neck. Probabilistic stimulus was applied to either the back or neck of male and female rats. Swallows were evoked by an oral water stimulus, and electromyographic (EMG) activity of the mylohyoid, thyroarytenoid, and thyropharyngeus muscles served as the primary outcome measure.ResultsGaussian frequency stimulation applied to the skin surface of the thoracic back elicited significant increases in EMG amplitude of all three swallow-related muscles. Neck stimulation elicited a significant increase in EMG amplitude of the thyroarytenoid during swallow, but not the mylohyoid or thyropharyngeus muscles.DiscussionWhile the targeted thoracic spinal segments T9-T10 have been investigated for enhancing respiration, the promotion of swallowing through back stimulation has not been previously studied. Furthermore, this study introduces a new probabilistic stimulus based on Gaussian distribution. Probabilistic stimuli have been reported to excel in nerve stimulation in previous research. The results demonstrate that back stimulation effectively facilitated swallow more than neck stimulation and suggest potential applications for swallowing rehabilitation.

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“…Swallowing is then triggered as all-or-none kinetic responses and the sensory mediation of swallowing is further modulated by excitatory or inhibitory synaptic inputs from higher brain centers. [1][2][3][4][5] Furthermore, the sensory afferent signals conveyed from the upper alimentary tract influence swallowing motor sequences as well as respiratory-swallowing coordination, providing suitable modulation of swallowing-related motor activities to adapt to the rheological properties of the bolus transit. [6][7][8] Oropharyngeal dysphagia remains a critical cause of morbidity and mortality in the elderly population.…”

Section: Introductionmentioning

confidence: 99%

“…Afferent inputs from the pharynx and larynx are transmitted to the Sw‐CPG via the glossopharyngeal (GPN) and superior laryngeal nerves (SLNs). Swallowing is then triggered as all‐or‐none kinetic responses and the sensory mediation of swallowing is further modulated by excitatory or inhibitory synaptic inputs from higher brain centers 1–5 . Furthermore, the sensory afferent signals conveyed from the upper alimentary tract influence swallowing motor sequences as well as respiratory‐swallowing coordination, providing suitable modulation of swallowing‐related motor activities to adapt to the rheological properties of the bolus transit 6–8 …”

Section: Introductionmentioning

confidence: 99%

Sustained Effects of Capsaicin Infusion into the Oropharynx on Swallowing in Perfused Rats

Kaneko,

Sugiyama,

Munekawa

et al. 2023

The Laryngoscope

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ObjectivesTo examine the sustained effects of oropharyngeal capsaicin stimulation on the regulation of swallowing, we recorded the swallowing‐related nerve activities during continuous infusion of capsaicin solution into the oropharynx.MethodsIn 33 in situ perfused brainstem preparation of rats, we recorded the activities of the vagus, hypoglossal, and phrenic nerves during fictive swallowing. The interburst intervals (IBIs) of the swallowing‐related nerves during sequential pharyngeal swallowing (sPSW) elicited by electrical stimulation of the superior laryngeal nerve (SLN) during concurrent capsaicin stimulation of 10, 1, and 0.1 μM (n = 28) were compared with those during oropharyngeal infusion of saline (control) (n = 5).ResultsThe IBIs during SLN‐induced sPSW were reduced at 5 min after initiation of continuous infusion of 10 and 1 μM capsaicin solution. The IBIs showed significant decreases to −25.8 ± 6.9%, −25.9 ± 5.3, −18.3 ± 3.7, and −12.0 ± 1.6 at 30 min following 1 μM capsaicin stimulation at SLN stimulus conditions at 5 Hz of 1.2 times threshold, 10 Hz of 40 μA, 5 Hz of 60 μA, and 10 Hz of 60 μA, respectively. Continuous capsaicin stimulation of 0.1 μM solution did not show significant sustained effects.ConclusionPharmacological stimulation of capsaicin could provide time‐dependent effects on the likelihood of swallowing, particularly subserving sustained facilitation of swallowing reflex with appropriate concentration of capsaicin.Level of EvidenceNA Laryngoscope, 2023

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Effect of pharmacological inhibition of the pontine respiratory group on swallowing interneurons in the dorsal medulla oblongata

Cited by 6 publications

References 53 publications

Postinspiratory complex acts as a gating mechanism regulating swallow-breathing coordination and other laryngeal behaviors

Postinspiratory complex acts as a gating mechanism regulating swallow-breathing coordination and other laryngeal behaviors

Stochastic electrical stimulation of the thoracic or cervical regions with surface electrodes facilitates swallow in rats

Sustained Effects of Capsaicin Infusion into the Oropharynx on Swallowing in Perfused Rats

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