Differential effects of targeted tongue exercise and treadmill running on aging tongue muscle structure and contractile properties

Abstract

Age-associated changes in tongue muscle structure and strength may contribute to dysphagia in elderly people. Tongue exercise is a current treatment option. We hypothesized that targeted tongue exercise and nontargeted exercise that activates tongue muscles as a consequence of increased respiratory drive, such as treadmill running, are associated with different patterns of tongue muscle contraction and genioglossus (GG) muscle biochemistry. Thirty-one young adult, 34 middle-aged, and 37 old Fischer 344/Brown Norway rats received either targeted tongue exercise, treadmill running, or no exercise (5 days/wk for 8 wk). Protrusive tongue muscle contractile properties and myosin heavy chain (MHC) composition in the GG were examined at the end of 8 wk across groups. Significant age effects were found for maximal twitch and tetanic tension (greatest in young adult rats), MHCIIb (highest proportion in young adult rats), MHCIIx (highest proportion in middle-aged and old rats), and MHCI (highest proportion in old rats). The targeted tongue exercise group had the greatest maximal twitch tension and the highest proportion of MHCI. The treadmill running group had the shortest half-decay time, the lowest proportion of MHCIIa, and the highest proportion of MHCIIb. Fatigue was significantly less in the young adult treadmill running group and the old targeted tongue exercise group than in other groups. Thus, tongue muscle structure and contractile properties were affected by both targeted tongue exercise and treadmill running, but in different ways. Studies geared toward optimizing dose and manner of providing targeted and generalized tongue exercise may lead to alternative tongue exercise delivery strategies.

Figures

Fig. 1.

Maximal voluntary tongue force was significantly greater following 8 wk of targeted tongue exercise for each age group (P < 0.0001).

Fig. 2.

Endurance test times were significantly increased following 8 wk of treadmill running within the young adult rats (P = 0.047). There were not significant increases following the exercise period in the middle-age or old groups.

Fig. 3.

Progressive running test speeds significantly increased following 8 wk of targeted tongue exercise for each age group (P < 0.0001).

Fig. 4.

Maximal twitch tension was significantly greater in the young adult vs. middle-aged or old groups (P = 0.004).

Fig. 5.

Maximal tetanic tension was significantly greater in the young adult vs. middle-aged or old groups (P = 0.02).

Fig. 6.

Half-decay time was significantly shorter in the treadmill running group than the no exercise and targeted tongue exercise groups (P = 0.004).

Fig. 7.

Maximal twitch tension was significantly greater in the no exercise and targeted tongue exercise groups than the treadmill running group (P < 0.0001).

Fig. 8.

A significant interaction effect was found for fatigue index (P = 0.009). Post hoc testing revealed that there was significantly less fatigue in the young adult rats in the treadmill running group than in the no exercise group (P = 0.01). Post hoc testing also revealed that there was significantly less fatigue in the old rats within the targeted tongue exercise and treadmill running groups than in the old no exercise group (P < 0.0001; P = 0.0003, respectively). The old targeted tongue exercise group manifested the least fatigue overall.

Fig. 9.

Representative silver-stained SDS-PAGE gels from the genioglossus (GG) muscles of a young adult (A), middle-aged (B), and old (C) rat in the no exercise, targeted tongue exercise, and treadmill running groups.

Fig. 10.

Significant main effects for age were found for the myosin heavy chain (MHC) I, MHCIIx, and MHCIIb isoforms. The old group had a significantly greater proportion of MHCI than the young adult or middle-aged groups (P = 0.0466). The middle-aged and old groups had a significantly greater proportion of MHCIIx than the young adult group (P = 0.0004). The young adult group had a significantly greater proportion of MHCIIb than the middle-aged or old groups (P < 0.0001).

Fig. 11.

Significant main effects for experimental group were found for the MHCIIa, MHCIIb, and MHCI isoforms. The targeted tongue exercise group had a significantly greater proportion of MHCI than the no exercise or treadmill running groups (P = 0.001). The treadmill running group had a significantly lower proportion of MHCIIa and significantly higher proportion of MHCIIb than the no exercise or targeted tongue exercise groups (P < 0.0001; P = 0.003, respectively).