Asynchronous muscles

Last updated

Asynchronous muscles are muscles in which there is no one-to-one relationship between electrical stimulation and mechanical contraction. These muscles are found in 75% of flying insects and have convergently evolved 7-10 times. [1] Unlike their synchronous counterparts that contract once per neural signal, mechanical oscillations trigger force production in asynchronous muscles. Typically, the rate of mechanical contraction is an order of magnitude greater than electrical signals. [1] Although they achieve greater force output and higher efficiency at high frequencies, they have limited applications because of their dependence on mechanical stretch.

Contents

Structure

Molecular

Molecular components of myofibrils. Muscle can only contract when actin binding sites are revealed for myosin heads to attach. Created by Servier Medical Art and used under a Creative Commons Attribution 3.0 Unported License. Actin-myosin.png
Molecular components of myofibrils. Muscle can only contract when actin binding sites are revealed for myosin heads to attach. Created by Servier Medical Art and used under a Creative Commons Attribution 3.0 Unported License.

The exact molecular mechanisms used by asynchronous muscles are unknown, but it is believed that asynchronous muscles have no unique molecular structures as compared to their synchronous counterparts. A study investigating the asynchronous power muscles in bumblebees with X-ray diffraction videos showed that actin and myosin alone are sufficient for generating asynchronous behavior. [2] This finding helps explain how asynchronous muscles independently evolved across insect taxa. [1] More recent work using similar X-ray diffraction techniques in Lethocerus discovered that troponin bridges may play a critical role in stretch activation. As the muscle is stretched, these bridges move tropomyosin to reveal myosin-actin binding sites. [3] The muscle can only produce force when these sites are activated.

Macroscopic

Several changes to asynchronous muscles' macroscopic structure provide it with high force production and efficiency at high contraction frequencies. A critical adaptation is that asynchronous muscles maintain a tonic level of calcium instead of cycling calcium between contractions. This is evident in their long twitch duration. This is due to relatively spare sarcoplasmic reticulum. Because of requirements for high force production, myofiber and myofibril diameters are increased and the large amount of ATP necessary leads to high mitochondria densities. [1] In Cotinus mutabilis, asynchronous muscles are composed of 58.1% myofibril, 36.7% mitochondria, and 1.6% sarcoplasmic reticulum. In comparison, synchronous muscles in Schistocerca americana are composed of 65% myofibril, 23.5% mitochondria and 9.6% sarcoplasmic reticulum. [1] Although synchronous muscle has a higher percentage of myofibril, the cross-sectional area of asynchronous myofibril is 3.7 μm2 as opposed to 0.82 μm2 in synchronous muscle for the previously described species. [1]

Properties

Asynchrony between electrical stimulation and muscle contraction

The defining characteristic of asynchronous muscles is that there is no direct relationship between neural activation and muscle contraction. Typically, the number of muscle contractions is an order of magnitude greater than the number of action potentials sent to the muscle. Instead of directly controlling force generation, neural signals maintain [Ca2+] above a threshold for stretch-activation to occur. [4] For asynchronous muscles, neural inputs are typically thought of as an "on-off" switch while mechanical stimulus leads to individual muscle contractions. However, recent studies using genetically engineered Drosophila revealed correlations between [Ca2+] and force production. [5] Further work has shown bilateral calcium asymmetries in Drosophila. [4] These results indicate that there is some level of neural control beyond a simple "on" or "off" state.

Delayed stretch activation and delayed shortening deactivation

Left: stress produced by asynchronous muscle under a stretch-hold-release-hold experiment. Right: stress-strain plot showing positive work production. The work generated is equal to the area enclosed by the work loop. Adapted from Josephson, Malamud & Stokes 2000. Stretch-activation stretch-hold-release-hold.jpg
Left: stress produced by asynchronous muscle under a stretch-hold-release-hold experiment. Right: stress-strain plot showing positive work production. The work generated is equal to the area enclosed by the work loop. Adapted from Josephson, Malamud & Stokes 2000.

Delayed stretch activation and delayed shortening deactivation allow asynchronous muscles to generate positive work under cyclic oscillations. [6] When the muscle shortens, force drops and continues dropping even when the muscle length remains constant. Similarly, when the muscle lengthens, force increases and continues increasing after the muscle length remains constant. [1] Because of these delays, the work produced by the muscle during shortening is greater than the work absorbed during lengthening, therefore producing positive work. In contrast, synchronous muscles absorb work under similar conditions. [1] Both types of muscles consume ATP to drive force production and produce work. [6]

Long twitch duration

Long twitch duration is a functional consequence of the macroscopic properties of asynchronous muscle. Because asynchronous muscle can generate power without cycling calcium between contractions, the required rate of calcium regulation is significantly slower. In addition to the reduction in sarcoplasmic reticulum, relatively large myofibril diameters lead to increased diffusion times of Ca2+.Under isometric twitch experiments, asynchronous muscle in Cotinus mutabilis were found to have a twitch duration of 125 ms. In the same study, synchronous muscle in Schistocerca americana had a twitch duration of 40 ms. [1] Therefore, asynchronous muscles respond slowly to neural stimulus. In the case of insect flight, electrical stimulation alone is too slow for muscle control. For Cotinus mutabilis, the twitch duration is ten times as long as a wingbeat period. [1]

Functional significance

Resonant properties

Asynchronous muscles produce work when they undergo mechanical oscillations provided there is sufficient Ca2+. [1] [6] This can be achieved in one of two ways. First, two antagonistic muscles can be configured with elastic structures such that the contraction of one muscle stretches the other, causing it to activate and vice versa. This configuration is found in the power muscles of flying insects. [7] Second, a single asynchronous muscle can deform an elastic element which then stretches the muscle and causes the muscle to contract again. This setup is used by Drosophila to oscillate mechanosensory organs known as halteres. [8] As long as neural stimulus turn the muscles "on", both systems will continue to oscillate. These systems can be thought of as resonant systems, for which the oscillation frequency is dependent on the elasticity, damping, and force applied to the system. [9]

In a simplified case, this can be thought of as a linearly damped harmonic oscillator, for which the damped resonant frequency is

The damping ratio, ζ , is dependent on c, the damping coefficient, m, the mass of the system, and k, the stiffness of the system as shown

Power-control tradeoffs

Asynchronous muscles sacrifice neural control and flexibility in exchange for high force production and efficiency. Given the long twitch duration of asynchronous muscle, neural control is too slow to power flight. For instance, the asynchronous muscles in Cotinus mutabilis contract ten times faster than expected given their twitch duration. [1] Because these muscles rely on stretch activation, they must be configured such that they can be stretched by an external force. Furthermore, they are only useful when evolutionary pressures select for a muscle that reactively contracts against an imposed stretch. For example, in grasping tasks, it would be detrimental for antagonist muscles to spontaneously contract. Despite these disadvantages, asynchronous muscles are beneficial for high frequency oscillations. They are more efficient than synchronous muscles because they do not require costly calcium regulation. [6] This allows for changes in their macroscopic structure for increased force production.

Applications

Asynchronous muscles power flight in most insect species. a: Wings b: Wing joint c: Dorsoventral muscles power the upstroke d: Dorsolongitudinal muscles (DLM) power the downstroke. The DLMs are oriented out of the page. Motion of Insectwing.gif
Asynchronous muscles power flight in most insect species. a: Wings b: Wing joint c: Dorsoventral muscles power the upstroke d: Dorsolongitudinal muscles (DLM) power the downstroke. The DLMs are oriented out of the page.

Insect flight

Miniaturization of insects leads to high wingbeat frequencies with midges reaching wingbeat frequencies of 1000 Hz. [10] Because of their high force production and efficiency, asynchronous muscles are used to power insect flight in 75% of species. These insects possess two pairs of antagonistic asynchronous muscles that produce the majority of the power required for flight. These muscles are oriented such that as one pair contracts, it deforms the thorax and stretches the other pair, causing the second pair to contract. [7] The same thoracic deformations oscillate the wings. By utilizing the elastic thorax to store and return energy during wing deceleration and subsequent acceleration, Drosophila is able to reduce energetic costs by 10%. [11] This leads to a highly-efficient resonant system.

When wingbeat frequencies match the resonant frequency of the muscle-thorax system, flight is most efficient. In order to change wingbeat frequencies to avoid obstacles or generate more lift, insects use smaller "control" muscles such as the pleurosternal muscles to stiffen the thorax. [9] From the equations in the Resonant properties section, it is clear that the natural frequency of the system increases with stiffness. Therefore, modulating the stiffness of the thorax leads to changes in wingbeat frequency.

Mammalian hearts

Although heart muscles are not strictly asynchronous, they exhibit delayed stretch activation properties. As cardiac muscle is lengthened, there is an instantaneous rise in force caused by elastic, spring-like elements in the muscle. After a time delay, the muscle generates a second rise in force, which is caused by delayed stretch activation as seen in purely asynchronous muscle. [12] This property benefits heart function by maintaining papillary muscle tension during the entire systolic cycle well after the electrical wave has passed. [12] Through stretch activation, the heart can rapidly adapt to changes in heart rates.

Bioinspired robotics

Because of challenges arising from miniaturization such as poor scaling of electric motors, researchers have turned towards insects to develop centimeter-scale flying robots. [13] Although the actuators in the RoboBee are not asynchronous, they use elastic elements to transmit forces from its "muscles" (piezoelectric actuators) to flap the wings. Similar to flying insects, they exploit resonance to improve efficiency by 50%. [14]

See also

Related Research Articles

<span class="mw-page-title-main">Halteres</span> Pair of small club-shaped insect organs

Halteres are a pair of small club-shaped organs on the body of two orders of flying insects that provide information about body rotations during flight. Insects of the large order Diptera (flies) have halteres which evolved from a pair of ancestral hindwings, while males of the much smaller order Strepsiptera (stylops) have halteres which evolved from a pair of ancestral forewings.

<span class="mw-page-title-main">Motor neuron</span> Nerve cell sending impulse to muscle

A motor neuron is a neuron whose cell body is located in the motor cortex, brainstem or the spinal cord, and whose axon (fiber) projects to the spinal cord or outside of the spinal cord to directly or indirectly control effector organs, mainly muscles and glands. There are two types of motor neuron – upper motor neurons and lower motor neurons. Axons from upper motor neurons synapse onto interneurons in the spinal cord and occasionally directly onto lower motor neurons. The axons from the lower motor neurons are efferent nerve fibers that carry signals from the spinal cord to the effectors. Types of lower motor neurons are alpha motor neurons, beta motor neurons, and gamma motor neurons.

The muscular system is an organ system consisting of skeletal, smooth, and cardiac muscle. It permits movement of the body, maintains posture, and circulates blood throughout the body. The muscular systems in vertebrates are controlled through the nervous system although some muscles can be completely autonomous. Together with the skeletal system in the human, it forms the musculoskeletal system, which is responsible for the movement of the body.

<span class="mw-page-title-main">Smooth muscle</span> Involuntary non-striated muscle

Smooth (soft) muscle is an involuntary non-striated muscle, so-called because it has no sarcomeres and therefore no striations. It is divided into two subgroups, single-unit and multiunit smooth muscle. Within single-unit muscle, the whole bundle or sheet of smooth muscle cells contracts as a syncytium.

<span class="mw-page-title-main">Skeletal muscle</span> One of three major skeletal system types that connect to bones

Skeletal muscles are organs of the vertebrate muscular system and typically are attached by tendons to bones of a skeleton. The muscle cells of skeletal muscles are much longer than in the other types of muscle tissue, and are often known as muscle fibers. The muscle tissue of a skeletal muscle is striated – having a striped appearance due to the arrangement of the sarcomeres.

<span class="mw-page-title-main">Sarcomere</span> Repeating unit of a myofibril in a muscle cell

A sarcomere is the smallest functional unit of striated muscle tissue. It is the repeating unit between two Z-lines. Skeletal muscles are composed of tubular muscle cells which are formed during embryonic myogenesis. Muscle fibers contain numerous tubular myofibrils. Myofibrils are composed of repeating sections of sarcomeres, which appear under the microscope as alternating dark and light bands. Sarcomeres are composed of long, fibrous proteins as filaments that slide past each other when a muscle contracts or relaxes. The costamere is a different component that connects the sarcomere to the sarcolemma.

In biology, a motor unit is made up of a motor neuron and all of the skeletal muscle fibers innervated by the neuron's axon terminals, including the neuromuscular junctions between the neuron and the fibres. Groups of motor units often work together as a motor pool to coordinate the contractions of a single muscle. The concept was proposed by Charles Scott Sherrington.

<span class="mw-page-title-main">Sarcoplasmic reticulum</span> Menbrane-bound structure in muscle cells for storing calcium

The sarcoplasmic reticulum (SR) is a membrane-bound structure found within muscle cells that is similar to the smooth endoplasmic reticulum in other cells. The main function of the SR is to store calcium ions (Ca2+). Calcium ion levels are kept relatively constant, with the concentration of calcium ions within a cell being 10,000 times smaller than the concentration of calcium ions outside the cell. This means that small increases in calcium ions within the cell are easily detected and can bring about important cellular changes (the calcium is said to be a second messenger). Calcium is used to make calcium carbonate (found in chalk) and calcium phosphate, two compounds that the body uses to make teeth and bones. This means that too much calcium within the cells can lead to hardening (calcification) of certain intracellular structures, including the mitochondria, leading to cell death. Therefore, it is vital that calcium ion levels are controlled tightly, and can be released into the cell when necessary and then removed from the cell.

<span class="mw-page-title-main">Muscle cell</span> Type of cell found in muscle tissue

A muscle cell, also known as a myocyte, is a mature contractile cell in the muscle of an animal. In humans and other vertebrates there are three types: skeletal, smooth, and cardiac (cardiomyocytes). A skeletal muscle cell is long and threadlike with many nuclei and is called a muscle fiber. Muscle cells develop from embryonic precursor cells called myoblasts.

Uterine contractions are muscle contractions of the uterine smooth muscle that can occur at various intensities in both the non-pregnant and pregnant uterine state. The non-pregnant uterus undergoes small, spontaneous contractions in addition to stronger, coordinated contractions during the menstrual cycle and orgasm. Throughout gestation, the uterus enters a state of uterine quiescence due to various neural and hormonal changes. During this state, the uterus undergoes little to no contractions, though spontaneous contractions still occur for the uterine myocyte cells to experience hypertrophy. The pregnant uterus only contracts strongly during orgasms, labour, and in the postpartum stage to return to its natural size.

<span class="mw-page-title-main">Frank–Starling law</span> Relationship between stroke volume and end diastolic volume

The Frank–Starling law of the heart represents the relationship between stroke volume and end diastolic volume. The law states that the stroke volume of the heart increases in response to an increase in the volume of blood in the ventricles, before contraction, when all other factors remain constant. As a larger volume of blood flows into the ventricle, the blood stretches cardiac muscle, leading to an increase in the force of contraction. The Frank-Starling mechanism allows the cardiac output to be synchronized with the venous return, arterial blood supply and humoral length, without depending upon external regulation to make alterations. The physiological importance of the mechanism lies mainly in maintaining left and right ventricular output equality.

<span class="mw-page-title-main">Striated muscle tissue</span> Muscle tissue with repeating functional units called sarcomeres

Striated muscle tissue is a muscle tissue that features repeating functional units called sarcomeres. The presence of sarcomeres manifests as a series of bands visible along the muscle fibers, which is responsible for the striated appearance observed in microscopic images of this tissue. There are two types of striated muscle:

Muscle fatigue is when muscles that were initially generating a normal amount of force, then experience a declining ability to generate force. It can be a result of vigorous exercise, but abnormal fatigue may be caused by barriers to or interference with the different stages of muscle contraction. There are two main causes of muscle fatigue: the limitations of a nerve’s ability to generate a sustained signal ; and the reduced ability of the muscle fiber to contract.

<span class="mw-page-title-main">Muscle contraction</span> Activation of tension-generating sites in muscle

Muscle contraction is the activation of tension-generating sites within muscle cells. In physiology, muscle contraction does not necessarily mean muscle shortening because muscle tension can be produced without changes in muscle length, such as when holding something heavy in the same position. The termination of muscle contraction is followed by muscle relaxation, which is a return of the muscle fibers to their low tension-generating state.

<span class="mw-page-title-main">T-tubule</span> Extensions in cell membrane of muscle fibres

T-tubules are extensions of the cell membrane that penetrate into the center of skeletal and cardiac muscle cells. With membranes that contain large concentrations of ion channels, transporters, and pumps, T-tubules permit rapid transmission of the action potential into the cell, and also play an important role in regulating cellular calcium concentration.

<span class="mw-page-title-main">Insect flight</span> Mechanisms and evolution of insect flight

Insects are the only group of invertebrates that have evolved wings and flight. Insects first flew in the Carboniferous, some 300 to 350 million years ago, making them the first animals to evolve flight. Wings may have evolved from appendages on the sides of existing limbs, which already had nerves, joints, and muscles used for other purposes. These may initially have been used for sailing on water, or to slow the rate of descent when gliding.

<span class="mw-page-title-main">Myofilament</span> The two protein filaments of myofibrils in muscle cells

Myofilaments are the three protein filaments of myofibrils in muscle cells. The main proteins involved are myosin, actin, and titin. Myosin and actin are the contractile proteins and titin is an elastic protein. The myofilaments act together in muscle contraction, and in order of size are a thick one of mostly myosin, a thin one of mostly actin, and a very thin one of mostly titin.

Within the muscle tissue of animals and humans, contraction and relaxation of the muscle cells (myocytes) is a highly regulated and rhythmic process. In cardiomyocytes, or cardiac muscle cells, muscular contraction takes place due to movement at a structure referred to as the diad, sometimes spelled "dyad." The dyad is the connection of transverse- tubules (t-tubules) and the junctional sarcoplasmic reticulum (jSR). Like skeletal muscle contractions, Calcium (Ca2+) ions are required for polarization and depolarization through a voltage-gated calcium channel. The rapid influx of calcium into the cell signals for the cells to contract. When the calcium intake travels through an entire muscle, it will trigger a united muscular contraction. This process is known as excitation-contraction coupling. This contraction pushes blood inside the heart and from the heart to other regions of the body.

<span class="mw-page-title-main">Work loop</span>

The work loop technique is used in muscle physiology to evaluate the mechanical work and power output of skeletal or cardiac muscle contractions via in vitro muscle testing of whole muscles, fiber bundles or single muscle fibers. This technique is primarily used for cyclical contractions such as cockroach walking., the rhythmic flapping of bird wings or the beating of heart ventricular muscle.

The study of animal locomotion is a branch of biology that investigates and quantifies how animals move.

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 Josephson, R.K.; Malamud, J.G.; Stokes, D.R. (15 September 2000). "Asynchronous muscle: a primer". Journal of Experimental Biology. 203 (18): 2713–2722. doi:10.1242/jeb.203.18.2713. PMID   10952872.
  2. ↑ Iwamoto, H.; Yagi, N. (13 September 2013). "The Molecular Trigger for High-Speed Wing Beats in a Bee". Science. 341 (6151): 1243–1246. Bibcode:2013Sci...341.1243I. doi: 10.1126/science.1237266 . PMID   23970560. S2CID   32645102.
  3. ↑ Perz-Edwards, Robert J.; Irving, Thomas C.; Baumann, Bruce A. J.; Gore, David; Hutchinson, Daniel C.; Kržič, Uroš; Porter, Rebecca L.; Ward, Andrew B.; Reedy, Michael K. (4 January 2011). "X-ray diffraction evidence for myosin-troponin connections and tropomyosin movement during stretch activation of insect flight muscle". Proceedings of the National Academy of Sciences. 108 (1): 120–125. doi: 10.1073/pnas.1014599107 . PMC   3017141 . PMID   21148419.
  4. 1 2 Wang, Qian; Zhao, Cuiping; Swank, Douglas M. (November 2011). "Calcium and Stretch Activation Modulate Power Generation in Drosophila Flight Muscle". Biophysical Journal. 101 (9): 2207–2213. Bibcode:2011BpJ...101.2207W. doi:10.1016/j.bpj.2011.09.034. PMC   3207158 . PMID   22067160.
  5. ↑ Gordon, Shefa; Dickinson, Michael H. (14 March 2006). "Role of calcium in the regulation of mechanical power in insect flight". Proceedings of the National Academy of Sciences. 103 (11): 4311–4315. Bibcode:2006PNAS..103.4311G. doi: 10.1073/pnas.0510109103 . PMC   1449689 . PMID   16537527.
  6. 1 2 3 4 Syme, D. A. (1 August 2002). "How to Build Fast Muscles: Synchronous and Asynchronous Designs". Integrative and Comparative Biology. 42 (4): 762–770. doi: 10.1093/icb/42.4.762 . PMID   21708773.
  7. 1 2 Boettiger, Edward G.; Furshpan, Edwin (June 1952). "The mechanics of flight movements in diptera". The Biological Bulletin. 102 (3): 200–211. doi:10.2307/1538368. JSTOR   1538368.
  8. ↑ Deora, Tanvi; Singh, Amit Kumar; Sane, Sanjay P. (3 February 2015). "Biomechanical basis of wing and haltere coordination in flies". Proceedings of the National Academy of Sciences. 112 (5): 1481–1486. Bibcode:2015PNAS..112.1481D. doi: 10.1073/pnas.1412279112 . PMC   4321282 . PMID   25605915.
  9. 1 2 Dickinson, Michael H; Tu, Michael S (March 1997). "The Function of Dipteran Flight Muscle". Comparative Biochemistry and Physiology Part A: Physiology. 116 (3): 223–238. doi:10.1016/S0300-9629(96)00162-4.
  10. ↑ Sotavalta, Olavi (June 1953). "Recordings of high wing-stroke and thoracic vibration frequency in some midges". The Biological Bulletin. 104 (3): 439–444. doi:10.2307/1538496. JSTOR   1538496.
  11. ↑ Dickinson, Michael H.; Lighton, John R. B. (7 April 1995). "Muscle Efficiency and Elastic Storage in the Flight Motor of Drosophila". Science. 268 (5207): 87–90. Bibcode:1995Sci...268...87D. doi:10.1126/science.7701346. JSTOR   2886498. PMID   7701346. Gale   A16845096 ProQuest   213567876.
  12. 1 2 Vemuri, Ramesh; Lankford, Edward B.; Poetter, Karl; Hassanzadeh, Shahin; Takeda, Kazuyo; Yu, Zu-Xi; Ferrans, Victor J.; Epstein, Neal D. (2 February 1999). "The stretch-activation response may be critical to the proper functioning of the mammalian heart". Proceedings of the National Academy of Sciences. 96 (3): 1048–1053. Bibcode:1999PNAS...96.1048V. doi: 10.1073/pnas.96.3.1048 . PMC   15348 . PMID   9927691.
  13. ↑ Wood, R.J. (April 2008). "The First Takeoff of a Biologically Inspired At-Scale Robotic Insect". IEEE Transactions on Robotics. 24 (2): 341–347. CiteSeerX   10.1.1.370.1070 . doi:10.1109/TRO.2008.916997. S2CID   6710733.
  14. ↑ Jafferis, Noah T.; Graule, Moritz A.; Wood, Robert J. (2016). "Non-linear resonance modeling and system design improvements for underactuated flapping-wing vehicles". 2016 IEEE International Conference on Robotics and Automation (ICRA). pp. 3234–3241. doi:10.1109/ICRA.2016.7487493. ISBN   978-1-4673-8026-3. S2CID   15100511.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.