Research reportDifferential response properties of peripherally and cortically evoked swallows by electrical stimulation in anesthetized rats
Introduction
Swallowing is considered an essential action for life as it provides two vital functions: alimentation and protection of the upper respiratory tract. Basic swallowing movements may be programmed by the central pattern generator (CPG) for swallowing, which is located in the lower brain stem (Jean, 2001). In humans (Dziewas et al., 2003, Michou and Hamdy, 2009, Shingai et al., 1989) and animals (Kitagawa et al., 2002, Sumi, 1969), the swallowing CPG can be activated through cortical input as well as sensory input from the pharynx and larynx.
In humans, a number of spatially and functionally distinct cortical regions are involved in swallowing, including activation of the insular cortex during voluntary swallowing (Martin et al., 2001). The importance of the insula is shown by clinical studies in which swallows were evoked in subjects with epilepsy via insular stimulation (Penfield and Faulk, 1955, Soros et al., 2011), and from a patient who developed dysphagia after acute perisylvian infarcts (Foix–Chavany–Marie opercular syndrome) involving the bilateral insular cortex (Singh et al., 2011). Although these reports strongly suggest a critical role of the insular cortex in swallowing, to our knowledge, few studies have systematically investigated this function (Jezzini et al., 2012).
Two major cortical masticatory regions have been reported in rats, an anterior area (A-area) and a posterior area (P-area) (Zhang and Sasamoto, 1990). The P-area is located in the insula, and we previously found that electrically stimulating this region induced swallowing with rhythmic jaw movements (RJMs) in anesthetized rats (Tsujimura et al., 2012a). In the current study, we successfully initiated swallowing by electrically stimulating the cortical swallowing area (Cx) within the insular cortex. Although peripheral and central inputs are capable of inducing swallowing, few studies have investigated how these two types of swallows are functionally different. Sumi studied peripherally and cortically evoked swallows from the same animal, and also showed facilitation of swallowing initiation with the combination of peripheral and cortical stimulation (Sumi, 1969). However, to our knowledge, no report has quantitatively compared peripherally and cortically evoked swallows. Thus, the first aim of the current study was to determine the differences between swallows induced by peripheral electrical stimulation of the superior laryngeal nerve (SLN) versus those induced by cortical electrical stimulation of Cx.
Initiation of the swallowing reflex is affected by peripheral input from mechanical, gustatory, thermal, and noxious receptors (Chee et al., 2005, Hamdy et al., 2003, Tsujimura et al., 2009, Tsujimura et al., 2011, Tsujimura et al., 2013). When chewing, bolus processing in the oral and pharyngeal cavity always precedes swallowing (Hiiemae and Palmer, 1999, Palmer et al., 1992), suggesting that initiation of swallowing may be inhibited by chewing. Experimentally, during cortically (A-area)-evoked RJMs that resemble chewing, SLN-evoked swallowing was inhibited in anesthetized rats (Tsujimura et al., 2012a). Although we reported that SLN-evoked swallowing is inhibited by A-area stimulation, the initiation of swallowing during chewing in awake humans occurs in the hypopharynx (Saitoh et al., 2007), which is mainly innervated by the SLN. Thus, we hypothesized that SLN-evoked swallowing is less inhibited by A-area stimulation than cortically-evoked swallows. The second aim of this study was to investigate the difference in the effect of A-area stimulation between SLN and Cx-evoked swallows.
Section snippets
Preparation
This study was reviewed and approved by the Niigata University Intramural Animal Care and Use Committee (82-2). Experiments were performed on 26 male Sprague-Dawley rats weighing between 250 and 350 g. Animals were anesthetized with urethane (1.3 g/kg, i.p.), and supplemented with urethane whenever necessary to maintain anesthesia at a level that resulted in total absence of the corneal reflex. Rectal temperature was maintained at 37–38 °C by a thermostatically controlled heating pad. A midline
Comparison of SLN- and Cx-evoked swallows
Stimulation sites for the Cx (n = 10) were identified histologically in the granular (GI), dysgranular (DI), and the dorsal part of agranular (AID) insular cortex according to the Paxinos and Watson stereotaxic atlas (Fig. 1) (Paxinos and Watson, 2006). Swallowing was evoked by electrical stimulation of the SLN and Cx (Fig. 2A). The threshold to elicit a swallow ranged from 6 to 80 μA for the SLN and from 60–210 μA for the Cx. The onset latency of the first swallow was significantly longer when
Discussion
In the present study, we found that aspects of swallowing differed depending on whether the triggering input was peripheral (SLN) or cortical (Cx). The onset latency of the first swallow and burst duration of the Thy muscle were significantly shorter and longer, respectively, when swallowing was evoked from the periphery compared with centrally. The most effective stimulation frequencies for SLN-evoked swallows were 30 Hz and 50 Hz, whereas it was only 10 Hz for Cx-evoked swallows. When SLN input
Conflict of interest
The authors declare that they have no conflict of interest.
Acknowledgements
This study was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (#24390431 to M.I. and #23792507 and #26870207 to T.T.), and by the Strategic Young Researcher Overseas Visits Program for Accelerating Brain Circulation (S2504) from the Japan Society for the Promotion of Science.
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