Neural Control of Skeletal Muscle - Animal...
2
540 Chapter 20 Neural Control of Skeletal Muscle Whole skeletal muscles in both vertebrates and invertebrates produce smooth, fluid movements that are physiologically and behaviorally useful. These movements are generated by continu ous and finely controlled neural input. Unlike smooth and cardiac muscles (which may generate contractions endogenously and may respond to hormonal as well as neural control), skeletal muscles contract only when stimulated by motor neurons. Two contrasting evolutional')' approaches are known to provide gradation of tension in a muscle, one exemplified by vertebrates (the vertebrate plan) and the other by arthropods (the arthropod plan). In most of the well- studied invertebrate groups other than arthropods, muscle tension is controlled by variations on the arthropod plan. The vertebrate plan is based on muscles organized into motor units A vertebrate skeletal muscle is innervated typically by about 100 to 1000 motor neurons. The axon of each motor neuron typically branches to innervate multiple muscle fibers, and each muscle fiber receives synaptic input from only one motor neuron. A mo tor neuron and all the muscle fibers it innervates are collectively termed a motor unit (Fig une 20.15). When the motor neuron gener ates an action potential, all of the muscle fibers in the motor unit generate action potentials and contract to produce a twitch. Trains of action potentials of increasing frequencies can produce sum mation of twitches up to fused tetanic contraction.10 Thus, as in whole muscles, the amount of tension produced by a single motor FIGURE 20.15 Vertebrate skeletal muscles consist of many different, independent motor units An action potential in the motor neuron of one motor unit stimulates an action potential and contraction in all of the muscle fibers it innervates. Varying the number of active motor units varies the amount of tension pro duced by the whole muscle. Spinal cord Gastrocnemius muscle of frog le<j KEY unit can be varied by varying the frequency of action potentials generated by the motor neuron. Although the amount of tetanic tension varies in different animals, in many vertebrate muscles it is only two to five times the twitch tension. A more dramatic effect on the amount of tension developed by a whole muscle can be accomplished by varying the number of active motor units. Increasing the number of active motor units is called recruitment of motor units. Recruitment requires stimulating increasing numbers of motor neurons that inneivate the muscle. For example, the tension in a muscle innervated by 100 motor neurons could be graded in 100 steps by recruitment. The amount of tension developed by the whole muscle increases as more motor units are activated (recruited). Recruitment is the dominant means used to control the amount of tension produced in vertebrate twitch muscles. Varying the number of active motor units, as wel 1 as the timing of their activation, ensures precise and smooth movements. The elastic properties of the muscle also contribute to the smoothness of movement. The innervation of vertebrate tonic muscle is intermediate between the general vertebrate and arthropod plans Whereas each fiber of a twitch muscle has a single synaptic contact near the middle of the fiber, each muscle fiber of a tonic muscle receives many branches of a motor neuron, so it has many synaptic contacts distributed over its length. This pattern, shown in Figure 20.16a, is termed multiterminal innervation. An action potential generated by a motor neuron produces an excitatory postsynaptic potential (EPSP) at each of the distributed junctions. The muscle fiber has little or no ability to generate action potentials. Each depolarizing EPSP spreads passively over a region of membrane and down the t-tubules in that area. Contraction occurs by excitation-contraction coupling. Because an EPSP is produced at each of the many terminals along the entire length of the fiber, the contractile elements along the entire fiber are activated. The amount of tension generated depends directly on the amount of depolarization produced by the EPSPs. The arthropod plan is based on multiterminal innervation of each muscle fiber by more than one neuron Although the fibers of arthropod skeletal muscles share many fea tures of vertebrate skeletal muscle, including the organization of thick and thin filaments into sarcomeres and excitation-contrac tion coupling by way of t-tubules and SR, they show interesting differences in their patterns of innervation. A typical arthropod whole muscle is innervated by one to ten motor neurons, in contrast to the hundreds or thousands of motor neurons that innervate a whole vertebrate muscle. Most individual arthropod muscle fibers are innervated by more than one motor neuron, a pattern termed polyneuronal innervation (Figure 20.166). As in tonic muscle, each neuron in arthropod skeletal muscle branches to provide multiterminal innervation. Arthropod muscle fibers typically do not generate all-or-none action potentials. (Insect flight muscles, which do generate action potentials, are an exception.) Because arthropod muscle fibers are innervated |n In mammals, fused tetanus occurs at about 300 action potentials/s in slow- twitch, oxidative muscle fibers, and at about 100 action potentials/s in fast-twit"1, glycolytic fibers.
Transcript of Neural Control of Skeletal Muscle - Animal...
540 Chapter 20
Neural Control of Skeletal MuscleWhole skeletal muscles in both vertebrates and invertebratesproduce smooth, fluid movements that are physiologically andbehaviorally useful. These movements are generated by continuous and finely controlled neural input. Unlike smooth and cardiacmuscles (which may generate contractions endogenously and mayrespond to hormonal as well as neural control), skeletal musclescontract only when stimulated by motor neurons. Two contrastingevolutional')' approaches are known to provide gradation of tensionin a muscle, one exemplified by vertebrates (the vertebrate plan) andthe other by arthropods (the arthropod plan). In most of the well-studied invertebrate groups other than arthropods, muscle tensionis controlled by variations on the arthropod plan.
The vertebrate plan is based on musclesorganized into motor unitsA vertebrate skeletal muscle is innervated typically by about 100to 1000 motor neurons. The axon of each motor neuron typicallybranches to innervate multiple muscle fibers, and each musclefiber receives synaptic input from only one motor neuron. A motor neuron and all the muscle fibers it innervates are collectivelytermed a motor unit (Fig une 20.15). When the motor neuron generates an action potential, all of the muscle fibers in the motor unitgenerate action potentials and contract to produce a twitch. Trainsof action potentials of increasing frequencies can produce summation of twitches up to fused tetanic contraction.10 Thus, as inwhole muscles, the amount of tension produced by a single motor
FIGURE 20.15 Vertebrate skeletal musclesconsist of many different, independentmotor units An action potential in the motorneuron of one motor unit stimulates an actionpotential and contraction in all of the musclefibers it innervates. Varying the number of activemotor units varies the amount of tension produced by the whole muscle.
Spinal cord
Gastrocnemiusmuscle of frog le<j
KEY
unit can be varied by varying the frequency of action potentialsgenerated by the motor neuron. Although the amount of tetanictension varies in different animals, in many vertebrate muscles itis only two to five times the twitch tension.
A more dramatic effect on the amount of tension developed by awhole muscle can be accomplished by varying the number of activemotor units. Increasing the number of active motor units is calledrecruitment of motor units. Recruitment requires stimulating increasingnumbers of motor neurons that inneivate the muscle. For example, thetension in a muscle innervated by 100 motor neurons could be gradedin 100 steps by recruitment. The amount of tension developed by thewhole muscle increases as more motor units are activated (recruited).Recruitment is the dominant means used to control the amount oftension produced in vertebrate twitch muscles. Varying the numberof active motor units, as wel 1 as the timing of their activation, ensuresprecise and smooth movements. The elastic properties of the musclealso contribute to the smoothness of movement.
The innervation of vertebrate tonic muscle isintermediate between the general vertebrateand arthropod plansWhereas each fiber of a twitch muscle has a single synaptic contactnear the middle of the fiber, each muscle fiber of a tonic muscle receivesmany branches of a motor neuron, so it has many synaptic contactsdistributed over its length. This pattern, shown in Figure 20.16a, istermed multiterminal innervation. An action potential generated by amotor neuron produces an excitatory postsynaptic potential (EPSP)at each of the distributed junctions. The muscle fiber has little or noability to generate action potentials. Each depolarizing EPSP spreadspassively over a region of membrane and down the t-tubules in thatarea. Contraction occurs by excitation-contraction coupling. Becausean EPSP is produced at each of the many terminals along the entirelength of the fiber, the contractile elements along the entire fiber areactivated. The amount of tension generated depends directly on theamount of depolarization produced by the EPSPs.
The arthropod plan is based on multiterminalinnervation of each muscle fiber by more thanone neuron
Although the fibers of arthropod skeletal muscles share many features of vertebrate skeletal muscle, including the organization ofthick and thin filaments into sarcomeres and excitation-contraction coupling by way of t-tubules and SR, they show interestingdifferences in their patterns of innervation. A typical arthropodwhole muscle is innervated by one to ten motor neurons, in contrastto the hundreds or thousands of motor neurons that innervate awhole vertebrate muscle. Most individual arthropod muscle fibersare innervated by more than one motor neuron, a pattern termedpolyneuronal innervation (Figure 20.166).
As in tonic muscle, each neuron in arthropod skeletal musclebranches to provide multiterminal innervation. Arthropod musclefibers typically do not generate all-or-none action potentials.(Insect flight muscles, which do generate action potentials, arean exception.) Because arthropod muscle fibers are innervated
|n In mammals, fused tetanus occurs at about 300 action potentials/s in slow-twitch, oxidative muscle fibers, and at about 100 action potentials/s in fast-twit"1,glycolytic fibers.
Musc le 541
; (,i) \'ertebrate tonic muscle fibers (b) Arthropod muscle fibers
Excitatory neurons Inhibitory neuron
Overlappingmotor units
nnervation euronal, multiterminal innervation
FIGURE 20.16 Innervation patterns of vertebrate tonic muscle fibers and arthropodmuscle fibers (a) Each vertebrate tonic muscle fiber is innervated by a single axon thatbranches to make many synaptic contacts along the length of the fiber. Tonic fibers do notproduce action potentials, (b) Each arthropod muscle fiber receives multiple synaptic contacts from several different neurons, some of which may be inhibitory. These muscle fibersoften do not produce action potentials. Muscles innervated according to the arthropod planhave overlapping motor units.
pi ilyneuronally, the motor units of arthropods overlap; each musclefiber is part of several motor units. Thus arthropods have only afew overlapping motor units per muscle, whereas vertebrates havemany, nonoverlapping motor units per muscle.
Some arthropod muscles are innervated by both excitatoryand inhibitory motor neurons. This feature—distinctly differentfrom vertebrate muscles, which are innervated solely by excitatoryneurons—allows peripheral inhibition. In arthropods, the excitatorytransmitter is typically glutamate (not acetylcholine) and the inhibitor)' transmitter is gamma-aminobutyric acid (GABA). Thealgebraic summation of graded inhibitory postsynaptic potentials(IPSPs) and EPSPs in the muscle fiber determines the amount of
{tension developed. The greater the depolarization, the greater theamount of Ca2+ released from the SR, and the greater the tensiondeveloped. Thus the dominant mechanism for controlling tension inarthropod muscles is controlling the degree of depolarization of musclefibers, which in turn depends on the frequency of action potentialsin the excitatory and inhibitory motor neurons.
Arthropod muscle fibers have a range of speeds of contraction,but unlike in vertebrate fibers, the velocity of contraction of arthropod muscle fibers is associated with different sarcomere lengths:Shi irt-sarcomere fibers contract quickly; and long-sarcomere fiberscontract slowly. Most arthropod muscles contain a variety of fiberswith different sarcomere lengths and contraction speeds. Somemuscles, however, are composed of all long-sarcomere slow fibers orall short-sarcomere fast fibers. For example, the muscles of crayfishand lobsters that control flexion and extension of the abdomen aremade up of either all fast or all slow fibers. Thus there are fast andslow flexor muscles and fast and slow extensor muscles. The slowflexor and extensor muscles each receive up to five excitatory motor neurons and one inhibitory neuron. Many of the fast musclesreceive three excitatory axons and one inhibitory axon.
An additional pattern of innervation is foundonly in insects. The skeletal muscles in insectsreceive synaptic input not only from excitatoryand inhibitory neurons but also from a third typeof neuron that releases octopamine or tyramine.The octopamine/tyramine transmitters do notdirectly trigger or inhibit muscle contraction,but instead perform two different functionsthat affect muscle activity. First, they modulateneuromuscular activity elicited by input fromglutamatergic excitatory motor neurons andGABA-ergic inhibitory neurons. For example,octopamine accelerates the relaxation rate ofmuscles by influencing the functions of chloride and potassium channels in the musclemembrane. Second, the octopamine/tyramineneurons to skeletal muscle fibers also promoteglycolysis, and therefore ATP production fromcarbohydrates, during contractions. This directneural control of metabolism plays an adaptiverole in adjusting muscle ATP production to theenergy demands of motor behaviors. Sometimes,however, it is not adaptive to use carbohydratesas metabolic fuel. Indeed, the flight muscles ofcertain insects that possess synchronous flightmuscles (see Box Extension 20.2) switch from
carbohydrate to lipid metabolism during long flights. For example,locusts have synchronous flight muscles and are well known fortheir ability to fly across oceans. In these animals, the octopamineneurons to the flight muscles stimulate glycolysis of carbohydratestores during rest, but the neurons are inhibited during flight. Inthe absence of octopamine input, the flight muscles metabolizelipids instead of carbohydrates.
SUMMARY Neural Control of SkeletalMusc le
■ The neuromuscular organization of vertebrates is characterizedby many nonoverlapping motor units, each controlled by a singlemotor neuron. Each muscle fiber within a motor unit generates anaction potential that spreads rapidly over the entire cell membraneand triggers the contractile response.
J Vertebrate tonic fibers usually do not generate action potentials.Each fiber is typically innervated by a single motor neuron thatmakes multiple synaptic contacts along its length.
■ The neuromuscular organization of arthropods is characterized byfew motor neurons, overlapping motor units, and in some cases,by peripheral inhibition. Each muscle fiber is typically innervatedby more than one motor neuron, and each neuron makes multiplesynaptic contacts on the fiber. Arthropod muscle fibers typicallydo not generate action potentials. Instead, the postsynapticpotentials produced at several points along the length of the fiberprovide graded electric signals that each trigger the contractilemachinery in a small section of the fiber and control the degreeof tension developed. Insect muscles are innervated not only byexcitatory and inhibitory neurons but also by neurons that releaseoctopamine or tyramine at synaptic contacts. These transmittersmodulate neuromuscular activity and regulate energy metabolism.
