Fish axial muscle is weird. It's so weird that Sven Gemballa and Felix Vogel, in their December paper in Comparative Biochemistry and Physiology, are the first to attempt to explain its three-dimensional structure since R. McNeill Alexander in 1969. Its complexity has long frustrated fish biologists because there's been no direct way to link muscle properties to body bending. Alexander described a spiral pattern in muscle fibre orientation, which might allow all fibres to shorten the same amount. His study, however, was fairly theoretical and did not indicate how the muscle force would be transmitted to the skeleton. Gemballa and Vogel's study,covering 26 species spanning the range of fish diversity, is the first to offer detailed evidence for a general bending mechanism in fishes.
Unlike in tetrapods, whose muscles tend to be separate units with fairly consistent fibre angles, fish white muscle is arranged down the body in nested W-shaped blocks, with the centre of the W pointing forward. The blocks, called myomeres, are separated by collagenous sheets called myosepta. Between the myosepta, the muscle fibres themselves also have a complex arrangement.
Using techniques ranging from electron microscopy to manual microdissections, Gemballa and Vogel tracked muscle fibres from one myoseptum to the next. They then dissected out the myosepta and used polarized light microscopy to visualize regions of parallel collagen fibres that indicate force direction and how those forces might be transmitted to the skeleton. This process produces an integrated model of the bending mechanism.
Although Gemballa and Vogel found essentially the same arrangement that Alexander described, with fibres spiralling down the body, they interpret it differently. Alexander hypothesized that the spiral allowed all muscle fibres to contract by about the same amount. Gemballa and Vogel instead divide it into two parts that wrap around each other like DNA's double helix. The outside portion of the helices – one strand of the `DNA' – which they term the helical muscle fibre arch, forms an arch from the body's centre line out to the left or right side and back again. Passing under that arch is a central portion of the helix – the other `DNA' strand – called the crossing muscle fibres. They hypothesize that the crossing muscle fibres,like a pulley, support the helical muscle arch when it bends the fish's body.
Paradoxically, these arches are located anteriorly, but they cause bending mostly near the tail. In explanation, Gemballa and Vogel describe different fibre and tendon orientations near the tail that could help transmit bending forces posteriorly. The fibres lose their helical pattern and instead, like a pinnate muscle, attach to tendons running towards the tail to efficiently transfer force backwards.
Gemballa and Vogel's most important contribution, however, may be their description of myoseptal tendons. These tendon-like thickenings in the myosepta may help muscle fibres from consecutive myomeres to act together as helices. By observing the tendon orientations, they estimate force directions in the myosepta. One tendon, the lateral band, approximately follows the helical muscle fibre arch, indicating that forces are indeed produced along that trajectory. This lateral band may also transfer force from the arch fibres towards the vertebral column during locomotion.
Because of the complex arrangement of myomeres, myosepta and muscle fibres,the mechanical linkage between muscle shortening and body bending in swimming fish has been very unclear. By relating muscle fibre and myoseptal tendon orientations, Gemballa and Vogel start to make the link between muscle structure and function in the biomechanics of fish swimming.