Swallowing and Respiration: Shared Neural Substrates

Karen M. Wheeler, M.A., CCC-SLP
Christine M. Sapienza, Ph.D., CCC-SLP
Department of Communication Sciences and Disorders
University of Florida

And

Malcom Randall V.A. Medical Center
Brain Rehabilitation and Research Center
Gainesville, FL

Abstract

It has become clear in the past 15 years that the relationship between respiration and swallowing is more integrated than previously thought, which is illustrated by the extent of coordination of swallowing events in specific parts of the respiratory cycle. Interestingly, these two functions share not only peripheral anatomical space within the aerodigestive tract, but also areas of control at the level of the central nervous system.

Neural control centers for both respiration and swallowing have been identified in animals and in humans; included are cortical, limbic, subcortical, and brainstem structures. These areas have been identified using methods such as functional magnetic resonance imaging (fMRI), positron emissions tomography (PET), magnetoencephalography (MEG), and transcranial magnetic stimulation (TMS). Additionally, the impact of lesions and aging to central and peripheral sites has been documented with regard to effects on respiration and swallowing, and their overall coordination. It is suggested that evaluation of respiration and swallowing should not be mutually exclusive, and that combined evaluation may disseminate information which may be more clinically relevant than examination of either system independently.

Introduction

Swallowing is a complex neuromuscular activity involving rapid coordination of structures in the oral cavity, pharynx, and larynx. These structures also support respiration. In a very obvious sense, swallow and respiration are intimately connected by virtue of the fact that they share common anatomical space in the upper airway, or aerodigestive tract.

However, beginning approximately half a century ago with investigations involving animals, it was postulated and demonstrated that peripheral anatomical location is not the sole commonality between these two functions (Hukuhara & Okada, 1956; Kawasaki, Ogura, & Takenouchi, 1964). Rather what has been observed is the act of swallowing occurring at consistent points in the respiratory cycle. Further, it has been shown that while the onset of a swallow may interrupt inspiratory or expiratory phases of the respiratory cycle, approximately 95% of swallows end with expiration (Feroah et al., 2002; Klahn & Perlman, 1999; Martin-Harris et al., 2005; Martin-Harris, Brodsky, Price, Michel, & Walters, 2003; Martin, Logemann, Shaker, & Dodds, 1994; Perlman, He, Barkmeier, & Van Leer, 2005; Preiksaitis & Mills, 1996; Smith, Wolkove, Colacone, & Kreisman, 1989). This relatively invariant coordinated pattern of respiration and swallowing has led to questions about the networks of connections between the respiratory and swallow central neural systems.

Cortical control

Cortical control of swallowing

Volitional swallowing recruits multiple cerebral centers (Dziewas et al., 2003; Hamdy et al., 1999; Hamdy et al., 1999; Huckabee, Deecke, Cannito, Gould, & Mayr, 2003; Martin, Goodyear, Gati, & Menon, 2001; Mosier & Bereznaya, 2001; Mosier et al., 1999; Watanabe, Abe, Ishikawa, Yamada, & Yamane, 2004; Zald & Pardo, 1999). Procedures such as neurosurgery, neuroimaging and transcranial magnetic stimulation (TMS) have contributed to the current database regarding the location and contribution of these different cortical structures to the control of swallowing.

Early studies performed during neurosurgical procedures employed intra-operative stimulation of the lateral aspects of the human motor cortex. This stimulation resulted in swallowing initiation movements (Penfield & Boldery, 1937). More recently, evidence has been found for primary motor and premotor involvement in the initiation and modulation of swallowing using TMS, magnetoencephalography (MEG), and positron emissions tomography (PET) scanning (Hamdy et al., 1996; Hamdy et al., 1999; Watanabe et al., 2004; Zald & Pardo, 1999). As well results from functional magnetic resonance imaging (fMRI) indicate cerebral areas of activation during volitional swallowing (Martin et al., 2001; Mosier, Liu, Maldjian, Shah, & Modi, 1999; Zald & Pardo, 1999).