Fiber architecture and histochemistry in the cat neck muscle, biventer cervicis

1988 ◽  
Vol 60 (1) ◽  
pp. 46-59 ◽  
Author(s):  
F. J. Richmond ◽  
J. B. Armstrong

1. Biventer cervicis (BC) is an anatomically complex muscle that is divided by tendinous inscriptions into five in-series compartments of motor units. We have analyzed the fiber architecture and fiber-type composition of these different compartments using microdissection and histochemical methods. 2. BC narrows as it runs rostrally, but its in-series compartments have similar cross-sectional areas. The tapered shape of BC comes about because tendinous inscriptions and the tendon of insertion are oriented obliquely and muscle fibers attach in a progressively offset fashion from the medial to the lateral muscle edge. 3. Individual compartments of BC differ from one another in their architecture. The rostral two compartments (1 and 2) contain fibers of similar length that run between two plates of tendinous tissue. Compartments 3 and 4 are divided into two or three in-parallel subvolumes whose fiber bundles differ in their lengths and sites of attachment. Compartment 5 is the most variable in its structure. In some cats it is separated from compartment 4 by a tendinous inscription, but in other cats, it blends with a dorsomedial part of compartment 4 to form a single subvolume. 4. The relative lengths of fibers in different compartments were analyzed when the head and neck were held in different postures. Fibers in rostromedial regions were stretched more effectively when the head was flexed at suboccipital joints, and appeared to be less sensitive to movements at lower cervical joints. Movements across lower cervical joints produced substantial length changes in caudolateral parts of BC. 5. Muscle fibers of different histochemical types were not distributed evenly within each muscle compartment. Slow, oxidative (SO) fibers accounted for the majority of fibers near the nuchal midline but for only 30%-45% of fibers in lateral muscle regions. Proportions of fast, glycolytic (FG) fibers were greatest in lateral regions. Fast, oxidative-glycolytic (FOG) fibers were distributed quite uniformly throughout each compartment. 6. The specialized architecture of BC may shape its physiological capabilities. The complex internal structures of different compartments may alter the length-tension properties of BC.(ABSTRACT TRUNCATED AT 400 WORDS)

1986 ◽  
Vol 55 (1) ◽  
pp. 147-162 ◽  
Author(s):  
J. M. Spielmann ◽  
E. K. Stauffer

The glycogen-depletion technique (17, 32) has been used to examine the functional and morphological relationships between single isolated motor units (MUs) and single isolated Golgi tendon organs (GTOs) that were excited by the MUs in the soleus muscle of the cat. All MUs whose twitch contraction generated a brisk discharge from the GTOs during the rising and plateau phase of force development had a muscle fiber attached specifically to the proximal end of the GTOs. A significant (P less than 0.05) linear relationship was found between GTO discharge rate and the cross-sectional area of the muscle fibers that connected to a receptor. This was true when the correlation was calculated between firing rate and 1) the cross-sectional area of the entire collection of muscle fibers that connected in series to the GTOs; and 2) for the cross-sectional areas of the individually depleted muscle fibers that inserted on the GTO sample. These findings support the notion that the most physiologically relevant input for GTOs arises from the MUs that are attached directly in-series with the receptor.


1988 ◽  
Vol 60 (1) ◽  
pp. 30-45 ◽  
Author(s):  
J. B. Armstrong ◽  
P. K. Rose ◽  
S. Vanner ◽  
G. J. Bakker ◽  
F. J. Richmond

1. The neck muscle biventer cervicis is supplied by five separate nerve bundles that originate from segments C2-C5 and enter the muscle at different rostrocaudal levels. We have used the glycogen-depletion method to investigate the distribution of muscle fibers supplied by each nerve bundle and also the extent of motor-unit territories supplied by single motoneurons in the C3 segment. 2. Prolonged intermittent stimulation of each nerve bundle produced glycogen depletion in a compartment of muscle fibers that ran only a fraction of the whole-muscle length. The depleted compartment was separated by tendinous inscriptions from adjacent, serially arranged compartments that were supplied by different nerve bundles. Thus the muscle was divided into five in-series compartments, arranged in the same rostrocaudal sequence as the nerves by which they were supplied. 3. Six fast, glycolytic (FG) and five fast, oxidative-glycolytic (FOG) motor units were depleted by repetitive intracellular stimulation of their antidromically identified motoneurons in the C3 segment. The fibers of each motor unit were confined to a striplike subvolume whose cross-sectional area was only 20-40% of that for the whole compartment in which it was located. Single motor units contained an average of 408 extrafusal fibers (range: 262-582 fibers), and these were distributed with an average density of 20 fibers/mm2 in cross sections through their motor domains. No significant differences were found between the numbers or densities of fibers in FG and FOG motor units. 4. The specialized in-series organization of compartments has functional implications because the forces generated by one compartment of motor units must be transmitted through other in-series compartments of muscle fibers rather than directly onto skeletal attachments. The confined distribution of muscle fibers belonging to a single motor unit suggests that an additional level of organization may exist within individual compartments. The implications of these features for the physiological behavior and neural control of biventer cervicis are discussed.


1987 ◽  
Vol 57 (6) ◽  
pp. 1730-1745 ◽  
Author(s):  
S. C. Bodine ◽  
R. R. Roy ◽  
E. Eldred ◽  
V. R. Edgerton

In 11 tibialis anterior muscles of the cat, a single motor unit was characterized physiologically and subsequently depleted of its glycogen through repetitive stimulation of an isolated ventral root filament. Muscle cross sections were stained for glycogen using a periodic acid-Schiff reaction, and single-fiber optical densities were determined to identify those fibers belonging to the stimulated motor unit. Innervation ratios were determined by counting the total number of muscle fibers in a motor unit in sections taken through several levels of the muscle. The average innervation ratios for the fast, fatigueable (FF) and fast, fatigue-resistant (FR) units were similar. However, the slow units (S) contained 61% fewer fibers than the fast units (FF and FR). Muscle fibers belonging to S and FR units were similar in cross-sectional area, whereas fibers belonging to FF units were significantly larger than fibers belonging to either S or FR units. Additionally, muscle fibers innervated by a single motoneuron varied by two- to eightfold in cross-sectional area. Specific tensions, based on total cross-sectional area determined by summing the areas of all muscle fibers of each unit, showed a modest difference between fast and slow units, the means being 23.5 and 17.2 N X cm-2, respectively. Variations in maximum tension among units could be explained principally by innervation ratio, although fiber cross-sectional area and specific tension did contribute to differences between unit types.


1990 ◽  
Vol 259 (3) ◽  
pp. C507-C514 ◽  
Author(s):  
B. Jiang ◽  
R. R. Roy ◽  
V. R. Edgerton

The metabolic plasticity of single fibers in adult cat medial gastrocnemius (MG) 6 mo after complete spinal cord transection (Sp) at T12-T13 was studied. Some Sp cats were trained to weight support (Sp-WS) 30 min/day beginning 1 mo posttransection. Cross-sectional area, succinate dehydrogenase (SDH), alpha-glycerophosphate dehydrogenase (GPD), and myofibrillar adenosinetriphosphatase (ATPase) activities were determined in fibers identified in frozen serial sections. Fibers were categorized as light or dark based on myosin ATPase staining, alkaline preincubation. The percentage of dark ATPase fibers was higher in Sp and Sp-WS (approximately 85%) than in control (approximately 60%). All dark ATPase fibers reacted positively to a fast myosin heavy chain monoclonal antibody. In both spinal groups, a higher percentage of dark ATPase fibers reacted to both fast and slow myosin heavy chain antibodies than in controls. Neither Sp nor Sp-WS cats showed fiber atrophy. Compared with control, SDH activity was decreased in both fiber types of Sp cats. Daily weight-support training ameliorated this adaptation. There were no differences among the three groups in mean GPD and ATPase activities for either fiber type. There was a slight tendency, however, for spinal cats to have higher GPD and ATPase activities (independent of type) than control, probably reflecting the larger proportion of dark ATPase fibers in these cats. These observations indicate that 6 mo after spinalization in adult cats, some of the fibers of a fast muscle became "faster" and developed oxidative and glycolytic enzyme profiles that normally are exhibited in fast fatigable motor units.(ABSTRACT TRUNCATED AT 250 WORDS)


1998 ◽  
Vol 84 (6) ◽  
pp. 2183-2189 ◽  
Author(s):  
Akihiko Ishihara ◽  
Roland R. Roy ◽  
Yoshinobu Ohira ◽  
Yasuhiko Ibata ◽  
V. Reggie Edgerton

There have been no systematic comparisons of skeletal muscle adaptations in response to voluntary wheel running under controlled loading conditions. To accomplish this, a voluntary running wheel for rats and mice was developed in which a known load can be controlled and monitored electronically. Five-week-old male Sprague-Dawley rats (10 rats/group) were assigned randomly to either a 1) sedentary control group (Control); 2) voluntary exercised with no load (Run-No-Load) group; or 3) voluntary exercised with additional load (Run-Load) group for 8 wk. The load for the Run-Load group was progressively increased to reach ∼60% of body weight during the last week of training. The proportions of fast glycolytic (FG), fast oxidative glycolytic (FOG), or slow oxidative (SO) fibers in the plantaris were similar in all groups. The absolute and relative plantaris weights were greater in the Run-Load group compared with the Control and Run-No-Load groups. The mean fiber cross-sectional areas of FG, FOG, and SO fibers were 20, 25, and 15% greater in the Run-Load than in Control rats. In addition, these fiber types were 16, 21, and 12% larger in Run-Load than in Run-No-Load rats. The muscle weights and mean cross-sectional areas of each fiber type were highly correlated with the average running distances and total work performed in the Run-Load, but not the Run-No-Load, group. The slope of the relationship between fiber size and running distance and total work performed was significant for each fiber type but was higher for FG and FOG fibers compared with SO fibers. These data show that the load on a rat running voluntarily can determine the magnitude of a hypertrophic response and the population of motor units that are recruited to perform at a given loading condition.


Development ◽  
1990 ◽  
Vol 109 (3) ◽  
pp. 723-732
Author(s):  
T. Fladby ◽  
J.K. Jansen

We studied the fiber type composition and contractile properties of mouse soleus motor units at 2 days, 5 days and 2 weeks of age. We used Lucifer Yellow injection to mark muscle fibers belonging to the same motor unit in the two youngest age groups, and the traditional method of glycogen depletion in the oldest. The age groups were chosen because 2 days is at the end of muscle fiber production; 5 days is at the start of synapse elimination in the muscle and 2 weeks is at the end. Muscle fibers were classified as fast (F) or slow (S) on the basis of their myosin heavy chain (MHC) content, as determined by different monoclonal antibodies. Motor units are already dominated by either F- or S-fibers at 2 days, suggesting an early preferential innervation of the two types of fibers. A substantial part of the remaining refinement of the innervation takes place during the next 3 days, while the total number of terminals in the muscle remains constant. This is most easily explained by an exchange of aberrant for correct synapses during this period. A smaller part of the refinement of the innervation occurs during the subsequent period of synapse elimination.


1990 ◽  
Vol 69 (3) ◽  
pp. 1150-1158 ◽  
Author(s):  
S. J. Hoffmann ◽  
R. R. Roy ◽  
C. E. Blanco ◽  
V. R. Edgerton

Do muscle fiber properties commonly associated with fiber types in adult animals and the population distribution of these properties require normal activation patterns to develop? To address this issue, the activity of an oxidative [succinic dehydrogenase (SDH)] and a glycolytic [alpha-glycerophosphate dehydrogenase (GPD)] marker enzyme, the characteristics of myosin adenosinetriphosphatase (myosin ATPase, alkaline preincubation), and the cross-sectional area of single fibers were studied. The soleus and medial gastrocnemius of normal adult cats were compared with cats that 6 mo earlier had been spinally transected at T12-T13 at 2 wk of age. In control cats, SDH activity was higher in dark than light ATPase fibers in the soleus and higher in light than dark ATPase fibers in the medial gastrocnemius. After transection, SDH activity was similar to control in both muscles. GPD activity appeared to be elevated in some fibers in each fiber type in both muscles after transection. The cross-sectional areas most affected by spinal transection were light ATPase fibers of the soleus and dark ATPase fibers of the medial gastrocnemius, the predominant fiber type in each muscle. These data demonstrate that although the muscle fibers of cats spinalized at 2 wk of age presumably were never exposed to normal levels of activation, the activity of an oxidative marker enzyme was maintained or elevated 6 mo after spinal transection. Furthermore, although the absolute enzyme activities in some fibers were elevated by transection, three functional protein systems commonly associated with fiber types, i.e., hydrolysis of ATP by myosin ATPase and glycolytic (GPD) and oxidative (SHD) metabolism, developed in a coordinated manner typical of normal adult muscles.


2003 ◽  
Vol 89 (2) ◽  
pp. 738-744 ◽  
Author(s):  
Eric J. Perreault ◽  
Scott J. Day ◽  
Manuel Hulliger ◽  
C. J. Heckman ◽  
Thomas G. Sandercock

Nearly all muscle models and most motor control concepts assume that forces from individual muscle fibers and motor units sum in an additive manner once effects of in-series tendon compliance are taken into account. Due to the numerous mechanical linkages between individual fibers, though, it is unclear whether this assumption is warranted. This work examined motor unit force summation over a wide range of muscle forces in the cat soleus. Nonadditive summation implies a nonlinear summation of motor unit forces. Summation nonlinearities were quantified during interactions of 10 individual motor units and 4 motor unit bundles containing approximately 10 units each. These protocols allowed motor unit force summation to be examined from approximately 0 to 25% of tetanic muscle force. Nonlinear summation was assessed by comparing the actual forces to the algebraic sum of individual units and bundles stimulated in isolation. Superadditive summation meant that the actual force exceeded the algebraic sum, whereas subadditive summation meant that the actual force was smaller than the algebraic sum. Experiments tested the hypothesis that superadditive summation occurs at low force levels when few motor units are recruited, whereas subadditive summation prevails above 10% of tetanic force. Results were consistent with this hypothesis. As in previous studies, nonlinear summation in the soleus was modest, but a clear transition from predominately superadditive to predominantly subadditive summation occurred in the range of 6–8% of tetanic force. The largest nonlinearities were transient and appeared at the onset of recruitment and derecruitment of groups of motor units. The results are discussed in terms of the mechanical properties of the connective tissue forming the tendon and linking muscle fibers.


1998 ◽  
Vol 84 (1) ◽  
pp. 318-326 ◽  
Author(s):  
Aladin M. Boriek ◽  
Charles C. Miller ◽  
Joseph R. Rodarte

Boriek, Aladin M., Charles C. Miller III, and Joseph R. Rodarte. Muscle fiber architecture of the dog diaphragm. J. Appl. Physiol. 84(1): 318–326, 1998.—Previous measurements of muscle thickness and length ratio of costal diaphragm insertions in the dog (A. M. Boriek and J. R. Rodarte. J. Appl. Physiol. 77: 2065–2070, 1994) suggested, but did not prove, discontinuous muscle fiber architecture. We examined diaphragmatic muscle fiber architecture using morphological and histochemical methods. In 15 mongrel dogs, transverse sections along the length of the muscle fibers were analyzed morphometrically at ×20, by using the BioQuant System IV software. We measured fiber diameters, cross-sectional fiber shapes, and cross-sectional area distributions of fibers. We also determined numbers of muscle fibers per cross-sectional area and ratio of connective tissue to muscle fibers along a course of the muscle from near the chest wall (CW) to near the central tendon (CT) for midcostal left and right hemidiaphragms, as well as ventral, middle, and dorsal regions of the left costal hemidiaphragm. In six other mongrel dogs, the macroscopic distribution of neuromuscular junctions (NMJ) on thoracic and abdominal diaphragm surfaces was determined by staining the intact diaphragmatic muscle for acetylcholinesterase activity. The average major diameter of muscle fibers was significantly smaller, and the number of fibers was significantly larger midspan between CT and CW than near the insertions. The ratio of connective tissues to muscle fibers was largest at CW compared with other regions along the length of the muscle. The diaphragm is transversely crossed by multiple scattered NMJ bands with fairly regular intervals offset in adjacent strips. Muscle fascicles traverse two to five NMJ, consistent with fibers that do not span the entire fascicle from CT to CW. These results suggest that the diaphragm has a discontinuous fiber architecture in which contractile forces may be transmitted among the muscle fibers through the connective tissue adjacent to the fibers.


Cells ◽  
2020 ◽  
Vol 9 (1) ◽  
pp. 197 ◽  
Author(s):  
Maria-Eleni Anagnostou ◽  
Russell T. Hepple

Skeletal muscle deteriorates with aging, contributing to physical frailty, poor health outcomes, and increased risk of mortality. Denervation is a major driver of changes in aging muscle. This occurs through transient denervation-reinnervation events throughout the aging process that remodel the spatial domain of motor units and alter fiber type. In advanced age, reinnervation wanes, leading to persistent denervation that accelerates muscle atrophy and impaired muscle contractility. Alterations in the muscle fibers and motoneurons are both likely involved in driving denervation through destabilization of the neuromuscular junction. In this respect, mitochondria are implicated in aging and age-related neurodegenerative disorders, and are also likely key to aging muscle changes through their direct effects in muscle fibers and through secondary effects mediated by mitochondrial impairments in motoneurons. Indeed, the large abundance of mitochondria in muscle fibers and motoneurons, that are further concentrated on both sides of the neuromuscular junction, likely renders the neuromuscular junction especially vulnerable to age-related mitochondrial dysfunction. Manifestations of mitochondrial dysfunction with aging include impaired respiratory function, elevated reactive oxygen species production, and increased susceptibility to permeability transition, contributing to reduced ATP generating capacity, oxidative damage, and apoptotic signaling, respectively. Using this framework, in this review we summarize our current knowledge, and relevant gaps, concerning the potential impact of mitochondrial impairment on the aging neuromuscular junction, and the mechanisms involved.


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