The limb muscles of a frog produce high levels of power to propel the animal into the air during a jump. To do this, they generate large forces quickly, and contract over relatively long distances (up to 30% of their resting length). However, the notion of muscles generating high forces while contracting over a large distance presents a bit of a conundrum because muscles have a relatively narrow range of lengths over which they generate their highest forces. It seems unlikely that muscles that shorten over great distances, like those in frog legs, will spend much time at lengths where forces can be maximized. Manny Azizi and Tom Roberts of Brown University recently addressed this conundrum and, in the process, revealed some surprising results.
Using bullfrogs, Azizi and Roberts chose to measure in vivo activation patterns and length changes in the major ankle extending plantaris muscle during jumping. Following these jumping trials, they used an in vitro preparation to determine a force–length curve for each muscle they measured in vivo. Force–length curves describe how a muscle's length affects its capacity for generating force. They consist of three parts: (1) an ‘ascending limb’ where force capacity increases as muscles go from short to intermediate lengths, (2) a plateau at intermediate lengths where muscles can maximize force production and (3) a ‘descending limb’, where further stretching leads to decreased forces. Azizi and Roberts wanted to know where the plantaris was operating in relation to its force–length properties as it contracted during a jump. They predicted that the muscle would start near its optimal length and move down its ascending limb as it shortened during contraction. But they were wrong.
Prior to a jump, it turns out the plantaris is resting at a relatively long length, positioned on the descending limb of its force–length curve, well beyond its optimum length for generating force. During the jump, the muscle contracts enough to put it onto the plateau of its force–length curve – in short, the plantaris ascends its descending limb. The authors were also able to show that this particular shortening pattern, where the muscle starts stretched and ends up at intermediate, optimal lengths, generates higher forces than the alternative strategy of starting at optimal lengths and contracting from there.
These are surprising results! Operating at such long lengths is, or I should say was, considered an anathema for muscles. But this view may be mammal-centric. In mammals, passive tension in stretched muscles increases very rapidly, and it is almost absurd to think of mammalian muscle starting to contract at the sorts of lengths these frog muscles are using regularly (1.33 resting length). However, as Azizi and Roberts show, passive tension in frog muscles stretched to this degree is quite low, allowing them to operate safely at such long lengths. The next time you find a frog, look closely at how the thigh, lower leg and foot are folded on top of one another, and remember that this seemingly awkward limb positioning is likely critical for stretching the underlying muscles so that they can contract over large distances without losing too much force.
