The muscle fiber type-fiber size paradox: hypertrophy or oxidative metabolism?

An inverse relationship exists between striated muscle fiber size and its oxidative capacity. This relationship implies that muscle fibers, which are triggered to simultaneously increase their mass/strength (hypertrophy) and fatigue resistance (oxidative capacity), increase these properties (strength or fatigue resistance) to a lesser extent compared to fibers increasing either of these alone. Muscle fiber size and oxidative capacity are determined by the balance between myofibrillar protein synthesis, mitochondrial biosynthesis and degradation. New experimental data and an inventory of critical stimuli and state of activation of the signaling pathways involved in regulating contractile and metabolic protein turnover reveal: (1) higher capacity for protein synthesis in high compared to low oxidative fibers; (2) competition between signaling pathways for synthesis of myofibrillar proteins and proteins associated with oxidative metabolism; i.e., increased mitochondrial biogenesis via AMP-activated protein kinase attenuates the rate of protein synthesis; (3) relatively higher expression levels of E3-ligases and proteasome-mediated protein degradation in high oxidative fibers. These observations could explain the fiber type-fiber size paradox that despite the high capacity for protein synthesis in high oxidative fibers, these fibers remain relatively small. However, it remains challenging to understand the mechanisms by which contractile activity, mechanical loading, cellular energy status and cellular oxygen tension affect regulation of fiber size. Therefore, one needs to know the relative contribution of the signaling pathways to protein turnover in high and low oxidative fibers. The outcome and ideas presented are relevant to optimizing treatment and training in the fields of sports, cardiology, oncology, pulmonology and rehabilitation medicine.

Postnatal development of fiber type composition in rabbit jaw and leg muscles.

We examined the difference in fiber type composition and cross-sectional areas during postnatal development in male rabbit jaw muscles and compared these with changes in leg muscles. The myosin heavy chain (MyHC) content of the fibers was determined by immunohistochemistry. No fiber type difference was found between the jaw muscles in 20-week-old rabbits. However, the way this adult fiber type composition was reached differed between the muscles. The deep temporalis, medial pterygoid, and superficial masseter displayed an increase in alpha fibers during early and a decrease during late postnatal development. Other jaw muscles displayed an increase in alpha fibers during early development only. In contrast, alpha fibers were not found in the soleus, in which fiber type changes were completed at week 4. The gastrocnemius muscle did not change its fiber type composition. Initially, fibers in jaw-opening muscles had larger cross-sectional areas than in other muscles, but they increased less during development. Although there were no large differences in the fiber type composition of muscles in young adult rabbits, large differences were found in the jaw muscles, but not in the leg muscles, during development. In part, these developmental changes in fiber percentages within the jaw muscles can be explained by functional modifications in this muscle group. In the present study, the deep temporalis, medial pterygoid, and superficial masseter showed the most dramatic percent changes in fibers during postnatal development.

Is fiber-type composition related to daily jaw muscle activity during postnatal development?

AIM: Muscles containing large numbers of slow-contracting fibers are generally more active than muscles largely composed of fast fibers. This relationship between muscle activity and phenotype suggests that (1) changes in fiber-type composition during postnatal development are accompanied by changes in daily activity and (2) individual variations in fiber-type composition are related to similar variations in daily muscle activity. METHODS: The masseter and digastric muscles of 23 New Zealand White rabbits (young, juvenile and adult) were examined for their phenotype (myosin heavy chain content) and their daily activity (total daily number of activity bursts). RESULTS: During development, the masseter showed a strong increase in the number of fast-type fibers compared to the number of slow-type fibers. During development, also the number of powerful bursts in the masseter increased. The digastric showed no significant changes in fiber types or burst numbers. Within each muscle, across individual animals, no significant correlations (R < 0.70) were found between any of the fiber types and daily burst numbers in any of the age groups. CONCLUSIONS: The results suggest that activity-related influences are of relatively minor importance during development and that other factors are dominant in determining fiber-type composition.

Postnatal transitions in myosin heavy chain isoforms of the rabbit superficial masseter and digastric muscle.

We investigated the early (< 8 weeks) and late (> 8 weeks) postnatal development of the fibre type composition and fibre cross-sectional area in the superficial masseter and digastric muscle of male rabbits. It was hypothesized, first, that due to the transition between suckling and chewing, during early postnatal development the increase in the proportion of slow fibre types and in fibre cross-sectional areas would be larger in the masseter than in the digastric; and second, that due to the supposed influence of testosterone during late postnatal development, the proportion of slow fibre types in both muscles would decrease. Fibre types were classified by immunostaining according to their myosin heavy chain (MyHC) content. The proportion of slow fibre types significantly increased in the masseter, from 7% at week 1 to 47% at week 8, and then decreased to 21% at week 20, while in the digastric it increased from 5% in week 1 to 19% at week 8 and remained the same thereafter. The changes in the proportion of fast fibre types were the opposite. The remarkable increase and decrease in the proportion of slow fibre types in the masseter was attributed predominantly to MyHC-cardiac alpha fibres. During early development, the cross-sectional area of all fibres in both muscles increased. However, only the fast fibre types in the masseter continued to grow further after week 8. Before weaning, the fast fibre types in the digastric were larger than those in the masseter, but after week 8, they became larger in the masseter than in the digastric. In adult animals, masseter and digastric had the same percentage of fast fibre types, but these fibres were almost twice as large in masseter as in digastric.

Daily activity of the rabbit jaw muscles during early postnatal development.

Early postnatal development of the jaw muscles is characterized by the transition from suckling to chewing behavior. As chewing develops the jaw closing muscles become more powerful compared with the jaw openers. These changes are likely to affect the amount of daily muscle activity. Therefore, the purpose of this study was to characterize for a jaw opener (digastric) and jaw closer (masseter) the total duration of daily muscle activity (i.e. the duty time), and the daily burst numbers and lengths during early postnatal development. Using radiotelemetry the activity of these muscles was recorded in 10 young New Zealand White rabbits between three and eight weeks of age. Fiber-type composition was analyzed at eight weeks of age by determining the myosin heavy chain content of the fibers. During postnatal development both muscles showed no significant decrease or increase in their daily activity. However, the interindividual variation of the duty time and burst number significantly decreased. There were no significant differences between the digastric and masseter except for the most powerful activities at eight weeks of age, where the masseter showed a significantly higher duty time and burst number than the digastric. The masseter contained a higher number of slow-type fibers expressing myosin heavy chain-I and myosin heavy chain-cardiac alpha than the digastric. The present results suggest that the amount of jaw muscle activation is already established early during postnatal development, before the transition from suckling to chewing behavior. This amount of activation seems to be related to the number of slow-type fibers.

Fibre-type composition of rabbit jaw muscles is related to their daily activity.

Skeletal muscles contain a mixture of fibres with different contractile properties, such as maximum force, contraction velocity and fatigability. Muscles adapt to altered functional demands, for example, by changing their fibre-type composition. This fibre-type composition can be changed by the frequency, duration and presumably the intensity of activation. The aim of this study was to analyse the relationship between the spontaneous daily muscle activation and fibre-type composition in rabbit jaw muscles. Using radio-telemetry combined with electromyography, the daily activity of five jaw muscles was characterized in terms of the total duration of muscle activity (duty time) and the number of activity bursts. Fibre-type composition of the muscles was classified by analysing the myosin heavy chain content of the fibres. The amount of slow-type fibres was positively correlated to the duty time and the number of bursts only for activations exceeding 20-30% of the maximum activity per day. Furthermore, cross-sectional areas of the slow-type fibres were positively correlated to the duty time for activations exceeding 30% of the maximum activity. The present data indicate that the amount of activation above a threshold (> 30% peak activity) is important for determining the fibre-type composition and cross-sectional area of slow-type fibres of a muscle. Activation above this threshold occurred only around 2% of the time in the jaw muscles, suggesting that contractile properties of muscle fibres are maintained by a relatively small number of powerful contractions per day.

Burst characteristics of daily jaw muscle activity in juvenile rabbits.

Muscle activation varies with different behaviors and can be quantified by the level and duration of activity bursts. Jaw muscles undergo large anatomical changes during maturation, which are presumably associated with changes in daily muscle function. Our aim was to examine the daily burst number, burst length distribution and duty time (fraction of the day during which a muscle was active) of the jaw muscles of juvenile male rabbits (Oryctolagus cuniculus). A radio-telemetric device was implanted to record muscle activity continuously from the digastric, superficial and deep masseter, medial pterygoid and temporalis during maturation week 9-14. Daily burst characteristics and duty times were determined for activations, including both powerful and non-powerful motor behavior. All muscles showed constant burst numbers, mean burst lengths and duty times during the recording period. Including all behavior, the temporalis showed significantly larger daily burst numbers (205,000) and duty times (18.2%) than the superficial and deep masseter (90,000; 7.5%). Burst numbers and duty times were similar for the digastric (120,000; 11.1%) and medial pterygoid (115,000; 10.4%). The temporalis and deep masseter showed many short low activity bursts (0.05 s), the digastric showed many long bursts (0.09 s). For activations during powerful behaviors the superficial masseter and medial pterygoid had the largest burst numbers and duty times. Both muscles showed similar burst characteristics for all activation levels. It was concluded that activation of the jaw muscles is differently controlled during powerful and non-powerful motor behaviors and the functional organization of motor control patterns does not vary from 9 to 14 weeks of age.

Long-term registration of daily jaw muscle activity in juvenile rabbits.

Understanding control of muscles during various tasks and their adaptive changes requires information on all motor behavior used throughout the day. The total duration of muscle activity depends on the magnitude of its activation and can change during maturation. Therefore, the purpose of this study was to examine the duration of muscle activity (i.e. duty time) exceeding various activity levels in maturing jaw muscles. A telemetric device was implanted into nine juvenile male New Zealand White rabbits to continuously record muscle activity during maturation weeks 9-14. Electrodes were inserted into digastric, superficial and deep masseter, medial pterygoid, and temporalis muscles. Duty times (expressed as a percentage of time) were calculated for activation exceeding different levels (5-90%) of EMG peak activity per 24-h period. At 10 weeks of age, for activation exceeding the 5% level, the duty time of the temporalis (20.0+/-5.2%) was statistically significantly higher than that of the medial pterygoid (11.2+/-1.5%), digastric (11.0+/-5.1%), superficial (12.6+/-5.6%), and deep masseter (8.6+/-5.5%). Duty times declined with increasing activity level. For activation exceeding the 40% level the duty times of the superficial masseter and medial pterygoid were significantly higher than those of the other muscles. During maturation none of the muscles showed a significant change in duty time. However, for activation exceeding the 5% level, the inter-individual variation in duty time decreased significantly for the digastric, and superficial and deep masseter.

Variation in daily masticatory muscle activity in the rabbit.

The daily use of masticatory muscles remains largely unclear, since continuous recordings were limited in space and time. This study's purpose was to use radio-telemetry to examine daily muscle use and its inter- and intra-individual variations. A telemetric device was implanted into the rabbit masseter, and the transmitted signals were digitally stored for 7 days. Muscle use was analyzed by calculation of the total time each muscle was activated above 5, 20, and 50% of the day's peak activity. Rabbits (n = 6) spent only 2% of the time chewing. Muscles were activated up to 20% of the total time at levels exceeding 5% of peak activity, and only about 0.5% of the time in forceful behaviors utilizing 50% of maximum contraction. It can be concluded that daily muscle use remained constant during succeeding days, but differed significantly among muscle regions and individuals.