Differential response properties of peripherally and cortically evoked swallows by electrical stimulation in anesthetized rats

Highlights

• We compared cortically and peripherally evoked swallows by electrical stimulation.

• Cortically evoked swallows had longer latencies than peripherally evoked swallows.

• Thyrohyoid burst duration was longer during peripherally evoked swallows.

• A-area stimulation inhibited cortical swallows more than peripheral swallows.

• Electrically evoked cortical and peripheral swallows have different properties.

Abstract

We compared onset latency, motor-response patterns, and the effect of electrical stimulation of the cortical masticatory area between peripherally and cortically evoked swallows by electrical stimulation in anesthetized rats. The number of swallows and the motor patterns were determined using electromyographic recordings from the thyrohyoid, digastric, and masseter muscles. The onset latency of the first swallow evoked by electrical stimulation of the cortical swallowing area (Cx) was significantly longer than that evoked by stimulation of the superior laryngeal nerve (SLN). The duration of thyrohyoid burst activity associated with SLN-evoked swallows was significantly longer than that associated with either Cx-evoked or spontaneous swallows. Combining Cx with SLN stimulation increased the number of swallows at low levels of SLN stimulation. Finally, A-area (the orofacial motor cortex) stimulation inhibited Cx-evoked swallows significantly more than it inhibited SLN-evoked swallows. These findings suggest that peripherally and cortically evoked swallows have different response properties and are affected differently by the mastication network.

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.