Localization and Contractile Properties of Intrinsic Longitudinal Motor Units of the Rat Tongue

Abstract

Tongue dysfunction is a hallmark of many human clinical disorders, yet we lack even a rudimentary understanding of tongue neural control. Here, the location and contractile properties of intrinsic longitudinal motor units (MUs) of the rat tongue body are described to provide a foundation for developing and testing theories of tongue motor control. One hundred and sixty-five MUs were studied by microelectrode penetration and stimulation of individual motor axons coursing in the terminal portion of the lateral (retrusor) branch of the hypoglossal nerve in the rat. Uniaxial MU force was recorded by a transducer attached to the protruded tongue tip, and MU location was estimated by electromyographic (EMG) electrodes implanted into the anterior, middle, and posterior portions of the tongue body. All MUs produced retrusive force. MU twitch force ranged from 2-129 mg (mean = 35 mg) and tetanic force ranged from 9-394 mg (mean = 95 mg). MUs reached maximal twitch force in 8-33 ms (mean = 15 ms) and were resistant to fatigue; following 2 min of stimulation, MUs (n = 11) produced 78-131% of initial force. EMG data were collected for 105 MUs. For 65 of these MUs, the EMG response was confined to a single electrode location: for 26 MUs to the anterior, 21 MUs to the middle, and 18 MUs to the posterior portion of the tongue. Of the remaining MUs, EMG responses were observed in two (38/40) or all three (2/40) tongue regions. These data provide the first contractile measures of identified intrinsic tongue body MUs and the first evidence that intrinsic longitudinal MUs are restricted to a portion of tongue length. Localization of MU territory suggests a role for intrinsic MU in the regional control of the mammalian tongue observed during feeding and speech.

Tongue Movements in Feeding and Speech

“…This work suggests that the distinction between 'extrinsic' and 'intrinsic' muscles may be artificial, a position held by many working with the tongues of non-human mammals and implicit in Takemoto (2001). Recently, the functional anatomy of the hyolingual musculature, especially the intrinsic musculature of the tongue, has attracted substantial attention (DePaul and Abbs, 1996;Sutlive et al,1999Sutlive et al, , 2000Sokoloff, 2000), as has the interleaving of extrinsic and extrinsic muscle fibers (Takemoto, 2001). DePaul and Abbs (1996) examined the intrinsic tongue muscles of macaques.…”

Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation

“…Each side of the rat tongue body comprises over 3,000 motor units (Sokoloff, 2000(Sokoloff, , 2004, providing fine neuromotor control with subsequently great diversity of response. For 70 years (Abd-El Malek, 1938), lingual muscles have been categorized according to location (e.g., intrinsic vs. extrinsic) or presumed action (e.g., protrusor vs. retrusor).…”

“…Multiple muscles work concurrently to provide structural support and active force for mobility. Experimental evidence (Sokoloff, 2000) suggests that within the tongue body, where many fibers insert by means of complex interdigitation, different motor unit populations, not whole muscle organs, are output elements of the tongue motor system, and that proper investigation and description of tongue function must consider neurophysiological rather than pure morphological properties (Sokoloff, 2004).…”

Effect of Artificial Rearing on the Contractile Properties and Myosin Heavy Chain Isoforms of Developing Rat Tongue Musculature

“…Newborn mammals obtain all of their nutrients through nutritive suckling. It is just one of several vital processes including respiration, chewing, swallowing, and vocalization that require normal tongue muscle function (Lowe 1981;Sokoloff 2000). Nutritive suckling involves a protrusion of the tip of the tongue against the nipple, followed by a retraction to exert a milking or stroking movement from below (Pieper 1963).…”