Neuromuscular organization of the canine tongue.

Abstract

The tongue manipulates food while chewing and swallowing, dilates the airway during inspiration, and shapes the sounds of speech in humans. While performing these functions the tongue morphs through many complex shapes. At present it is not known how the muscles of the tongue perform these complex shape changes. The difficulty in understanding tongue biomechanics is partly due to gaps in our knowledge regarding the complex neuromuscular anatomy of the tongue. In this study the motor and sensory nerve anatomy of four canine tongues was studied with Sihler's stain, a technique that renders most of the tongue tissue translucent while counterstaining nerves. An additional tongue specimen was serially sectioned to provide a reference for the muscle structure of the tongue. The hypoglossal nerve (XII) has approximately 50 primary nerve branches that innervate all intrinsic and extrinsic tongue muscles. Two extrinsic muscles, the styloglossus and hyoglossus, are innervated by about three to four branches from the lateral division of the XII. The third extrinsic muscle, the genioglossus, is composed of oblique and horizontal compartments, which receive about ten nerve branches from the medial division of the XII. The intrinsic muscles are composed of many neuromuscular compartments. On each side, the superior longitudinal muscle had an average of 40 distinct muscle fascicles that spanned the length of the tongue. Each of the fascicles is supplied by a nerve branch. The inferior longitudinal muscle had a similar organization. Each of the transverse and vertical muscles is composed of over 140 separate muscle sheets, and every sheet is innervated by a separate terminal nerve. The muscle sheets from the vertical and transverse alternate their orientation 90 degrees throughout the length of the tongue. It is concluded that the intrinsic canine tongue muscles are actually composed of groups of neuromuscular compartments that are arranged in parallel (longitudinal muscles) or in a precise alternating sequence (transverse and vertical muscles). This arrangement suggests that the compartments from the different tongue muscles could cooperate to control the three-dimensional contractile state of their local area. This hypothesis could explain how many different tongue shapes are formed, and is supported by physiologic evidence.