The normal development of the complex neuromuscular system used to control tongue movement is critical to the immediate survival of all terrestrial mammals. Voluntary control in this motor system involves a sequence of neural and muscular events beginning in the motor cortex. Coordinated tongue movements are needed for eating (mastication and swallowing), drinking, licking (suckling), breathing, grooming and vocalization. Clinically, and in contrast to a normal developmental progression, premature human infants often need to be fed intravenously or with a nasogastric tube for extended periods of time (weeks or months) to insure their survival. Attempts to begin bottle feeding these infants can result in apnea, bradycardia, hypoxia, fatigue and agitation and there can also be the long term consequence of delayed oral feeding milestones which results in longer hospital stays. A later impact on motor speech has also been documented. It may be that the interrupted normal maturation of the neuromuscular control system for appropriate suckling plays an important role here. In addition, infants born at term who also need non-oral nutrition due to system disorders or surgical interventions may also exhibit delayed oral feeding. We propose, therefore, to continue our studies of rat hypoglossal nucleus anatomy and tongue muscle contractile measures with a new emphasis on system development. We also propose to add morphological and biochemical studies of individual developing tongue muscles. The normal development of this system, and its cortical control, will then be compared and contrasted to that in rat pups who have been fed, for varying postnatal times, using a gastric cannula. Some animals will experience a near total absence of suckling while others will have their normal suckling sequence interrupted. This has been termed """"""""artificial rearing"""""""" and is modeled on the human infant interventions mentioned above. New preliminary data indicates that artificial rearing from postnatal days 4 to 13 results in striking changes in tongue contractile strength, speed, endurance, muscle fiber diameter and a persistence of developmental myosin heavy chain (MHC) isoforms, similar to changes observed in other skeletal muscles after a period of disuse. These studies should help to lay a firm foundation for an understanding of how the hypoglossal motor system develops, especially since many aspects of its normal development have simply not yet been studied. In addition, we hypothesize that the neuroanatomical organization within the hypoglossal nucleus, muscle morphology plus MHC expression, muscle contractile characteristics and afferent input from the motor cortex are altered in animals that have been artificially reared. The degree to which each of these components is altered needs to be ascertained for a clearer view of this motor system and to delineate those postnatal time periods that are the most critical for normal development. It is also hoped, for the long run, that these basic findings can have an application for a speedier and more complete rehabilitation of human infants that are necessarily deprived of normal suckling and eating.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC002008-10
Application #
6751528
Study Section
Integrative, Functional and Cognitive Neuroscience 8 (IFCN)
Program Officer
Shekim, Lana O
Project Start
1994-06-01
Project End
2006-05-31
Budget Start
2004-06-01
Budget End
2005-05-31
Support Year
10
Fiscal Year
2004
Total Cost
$261,034
Indirect Cost
Name
Virginia Commonwealth University
Department
Anatomy/Cell Biology
Type
Schools of Medicine
DUNS #
105300446
City
Richmond
State
VA
Country
United States
Zip Code
23298
Moore, Wayne A; Goldberg, Stephen J; Shall, Mary S (2007) Effects of artificial rearing on contractile properties of genioglossus muscle in Sprague-Dawley rat. Arch Oral Biol 52:133-41
Smith, J Chadwick; McClung, J Ross; Goldberg, Stephen J (2006) Effects of 12 days of artificial rearing on morphology of hypoglossal motoneurons innervating tongue retrusors in rat. Anat Rec A Discov Mol Cell Evol Biol 288:280-5
Smith, J Chadwick; Moore, W Allen; Goldberg, Stephen J et al. (2006) Contractile properties and myosin heavy chain composition of rat tongue retrusor musculature show changes in early adulthood after 19 days of artificial rearing. J Appl Physiol 101:1053-9
Smith, J Chadwick; Goldberg, Stephen J; Shall, Mary S (2006) Myosin heavy chain and fibre diameter of extrinsic tongue muscles in rhesus monkey. Arch Oral Biol 51:520-5
Smith, J Chadwick; Goldberg, Stephen J; Shall, Mary Snyder (2005) Phenotype and contractile properties of mammalian tongue muscles innervated by the hypoglossal nerve. Respir Physiol Neurobiol 147:253-62
Smith, J Chadwick; McClung, J Ross; Goldberg, Stephen J (2005) Postnatal development of hypoglossal motoneurons that innervate the hyoglossus and styloglossus muscles in rat. Anat Rec A Discov Mol Cell Evol Biol 285:628-33
Smith, Lane; Tiba, M Hakam; Goldberg, Mary Ellen et al. (2004) Chronic implantation of transit-time flow probes on the ascending aorta of rodents. Lab Anim 38:362-70
Kinirons, Stacy A; Shall, Mary S; McClung, J Ross et al. (2003) Effect of artificial rearing on the contractile properties and myosin heavy chain isoforms of developing rat tongue musculature. J Neurophysiol 90:120-7
McClung, J Ross; Goldberg, Stephen J (2002) Organization of the hypoglossal motoneurons that innervate the horizontal and oblique components of the genioglossus muscle in the rat. Brain Res 950:321-4
Sutlive, T G; Shall, M S; McClung, J R et al. (2000) Contractile properties of the tongue's genioglossus muscle and motor units in the rat. Muscle Nerve 23:416-25

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