Olfactory Stimulation Successfully Improves Swallowing Function of Aged Rats Through Activating Central Neuronal Networks and Downstream DHPR-RyR-mediated Neuromuscular Activities

Yea-Tzy Chen; Li-You Chen; Ting-Yi Renn; Meng-Shan Cheng; Chi-Te Wang; Igor V Klimenkov; Nikolay P Sudakov; Wen-Chieh Liao; Yea-Jyh Chen; Hung-Ming Chang

doi:10.1093/gerona/glab229

Olfactory Stimulation Successfully Improves Swallowing Function of Aged Rats Through Activating Central Neuronal Networks and Downstream DHPR-RyR-mediated Neuromuscular Activities

J Gerontol A Biol Sci Med Sci. 2022 Feb 3;77(2):235-242. doi: 10.1093/gerona/glab229.

Authors

Yea-Tzy Chen^{1

2}, Li-You Chen³, Ting-Yi Renn⁴, Meng-Shan Cheng¹, Chi-Te Wang^{2

5}, Igor V Klimenkov⁶, Nikolay P Sudakov⁶, Wen-Chieh Liao³, Yea-Jyh Chen⁷, Hung-Ming Chang⁴

Affiliations

¹ Department of Speech Language Pathology and Audiology, College of Health Technology, National Taipei University of Nursing and Health Sciences, Taiwan.
² Department of Special Education, University of Taipei, Taiwan.
³ Department of Anatomy, College of Medicine, Chung Shan Medical University, Taichung, Taiwan.
⁴ Department of Anatomy and Cell Biology, School of Medicine, College of Medicine, Taipei Medical University, Taiwan.
⁵ Department of Otolaryngology Head and Neck Surgery, Far Eastern Memorial Hospital, Taipei, Taiwan.
⁶ Department of Cell Ultrastructure, Limnological Institute, Siberian Branch of the Russian Academy of Sciences, Irkutsk 664033, Russia.
⁷ School of Nursing, College of Health and Human Services, University of North Carolina at Wilmington, USA.

PMID: 34378774
DOI: 10.1093/gerona/glab229

Abstract

Presbyphagia is age-related changes in swallowing function, which imposes a high risk of aspiration in older adults. Considering olfactory stimulation (OS) can influence behavioral activities by modulating neuronal excitability, the present study aims to determine whether OS could improve the swallowing function of aged rats through activating the central neuronal networks and downstream muscular activities participated in the control of swallowing. Aged male Wistar rats received OS by inhaling a mixture of plant-based volatile molecules twice a day for 12 days were subjected to functional magnetic resonance imaging (fMRI) and c-fos, choline acetyltransferase (ChAT) immunostaining to detect the neuronal activities of the orbitofrontal cortex (OFC) and medullary nuclei engaged in swallowing control, respectively. The functional effects of OS on downstream pharyngeal muscle activity were examined by evaluating the dihydropyridine receptor-ryanodine receptor (DHPR-RyR)-mediated intramuscular Ca2+ expression, and analyzing the amplitude/frequency of muscle contraction, respectively. In untreated rats, only moderate signal of fMRI and mild c-fos/ChAT expression was detected in the OFC and medullary nuclei, respectively. However, following OS, intense signals of fMRI and immunostaining were clearly expressed in the orbitofronto-medullary networks. Functional data corresponded well with above findings in which OS significantly enhanced DHPR-RyR-mediated intramuscular Ca2+ expression, effectively facilitated a larger amplitude of pharyngeal muscle contraction, and exhibited better performance in consuming larger amounts of daily dietary. As OS successfully activates the neuromuscular activities participated in the control of swallowing, applying OS may serve as an effective, easy, and safe strategy to greatly improve the swallow function of aging populations.

Keywords: DHPR; Olfactory stimulation; Orbitofronto-medullary networks; Pharyngeal muscle; Presbyphagia; RyR-mediated activity.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Calcium Channels, L-Type* / metabolism
Calcium* / metabolism
Deglutition
Male
Muscle, Skeletal / metabolism
Rats
Rats, Wistar
Ryanodine Receptor Calcium Release Channel / metabolism

Substances

Calcium Channels, L-Type
Ryanodine Receptor Calcium Release Channel
Calcium