Firing characteristics of swallowing interneurons in the dorsal medulla during physiologically induced swallowing in perfused brainstem preparation in rats

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

doi:10.1016/j.neures.2021.11.006

Cited by 8 publications

(10 citation statements)

References 49 publications

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“…S1). Swallow motor duration (R. W. Doty & Bosma, 1956) and interneurons in the dorsal swallow group (Yamamoto et al, 2022) respond similarly to fictive SLN stimulation and to physiological water-evoked swallows, though both involve sensory feedback mechanisms. 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).…”

Section: Discussionmentioning

confidence: 99%

“…Swallow motor duration (R. W. Doty & Bosma, 1956) and interneurons in the dorsal swallow group (Yamamoto et al, 2022) respond similarly to fictive SLN stimulation and to physiological water-evoked swallows, though both involve sensory feedback mechanisms. 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).…”

Section: Discussionmentioning

confidence: 99%

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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%

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

View full text Add to dashboard Cite

show abstract

“…Nucleus ambiguous innervates the muscles of the oral cavity, larynx, and pharynx through the trigeminal, facial, glossopharyngeal, vagus, and accessory nerves ( Petko and Tadi, 2023 ; Chandran and Doucet, 2024 ), The nucleus tractus solitary can receive incoming information from the nucleus doubtful and then send efferent fibers to the corresponding muscles, but mainly integrates information from higher cortical centers and peripheral sensory afferents and regulates swallowing according to the nature of the food bolus ( Chandran and Doucet, 2024 ; Ye et al, 2024 ). Overall (see Figure 1 ), the swallowing central pattern generator is responsible for the formation and regulation of swallowing motor sequences, processing incoming information, generating preprogrammed swallowing responses, and distributing appropriate signals to the motor nuclei of cranial nerves and their axons, which are ultimately transmitted to the many muscles involved in swallowing ( Yamamoto et al, 2022 ).…”

Section: Mechanisms Associated With Dysphagiamentioning

confidence: 99%

“… The mechanism of swallowing. As part of the swallowing central program generator, the nucleus ambiguous receives relevant cranial nerve stimulation and the nucleus tractus solitarius receives cortical and peripheral sensory input, after receiving the signal, the swallowing-related muscles are stimulated to promote the normal swallowing process ( Yamamoto et al, 2022 ). (A) The swallowing center’s operation.…”

Section: Mechanisms Associated With Dysphagiamentioning

confidence: 99%

The impact of physical therapy on dysphagia in neurological diseases: a review

Li,

Fu,

Xie

et al. 2024

Front. Hum. Neurosci.

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A neurogenic dysphagia is dysphagia caused by problems with the central and peripheral nervous systems, is particularly prevalent in conditions such as Parkinson’s disease and stroke. It significantly impacts the quality of life for affected individuals and causes additional burdens, such as malnutrition, aspiration pneumonia, asphyxia, or even death from choking due to improper eating. Physical therapy offers a non-invasive treatment with high efficacy and low cost. Evidence supporting the use of physical therapy in dysphagia treatment is increasing, including techniques such as neuromuscular electrical stimulation, sensory stimulation, transcranial direct current stimulation, and repetitive transcranial magnetic stimulation. While initial studies have shown promising results, the effectiveness of specific treatment regimens still requires further validation. At present, there is a lack of scientific evidence to guide patient selection, develop appropriate treatment regimens, and accurately evaluate treatment outcomes. Therefore, the primary objectives of this review are to review the results of existing research, summarize the application of physical therapy in dysphagia management, we also discussed the mechanisms and treatments of physical therapy for neurogenic dysphagia.

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“…15,16 Histological, electrophysiological, and immunohistochemical studies suggest that topical administration of TRPV1 agonist into the alimentary tract enhances the excitability of the swallowing reflex by activating swallowing-related neurons in the nucleus tractus solitarius and adjacent reticular formation in the dorsal medulla oblongata via afferent inputs from laryngeal fibers that show TRPV1 immunoreactivity in the nodose, petrosal, and jugular ganglia. 1,[17][18][19][20][21][22][23] Moreover, previous human studies have demonstrated that oropharyngeal stimulation by TRPV1 agonists accelerates the swallowing response, thereby improving swallowing function in dysphagic patients. [24][25][26][27][28] Conversely, sustained exposure to TRPV1 agonists lead to desensitization of vagal sensory fibers by depletion of neuropeptide including substance P, consequently resulting in a reduced sensitivity of swallowing reflex.…”

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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Firing characteristics of swallowing interneurons in the dorsal medulla during physiologically induced swallowing in perfused brainstem preparation in rats

Cited by 8 publications

References 49 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

The impact of physical therapy on dysphagia in neurological diseases: a review

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

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