Effects of task dynamics on coordination of the hand muscles and their adaptation to targeted muscle assistance

Dynamic characteristics of a manual task can affect the control of hand muscles due to the difference in biomechanical/physiological characteristics of the muscles and sensory afferents in the hand. We aimed to examine the effects of task dynamics on the coordination of hand muscles, and on the motor adaptation to external assistance. Twenty-four healthy subjects performed one of the two types of a finger extension task, isometric dorsal fingertip force production (static) or isokinetic finger extension (dynamic). Subjects performed the tasks voluntarily without assistance, or with a biomimetic exotendon providing targeted assistance to their extrinsic muscles. In unassisted conditions, significant between-task differences were found in the coordination of the extrinsic and intrinsic hand muscles, while the extrinsic muscle activities were similar between the tasks. Under assistance, while the muscle coordination remained relatively unaffected during the dynamic task, significant changes in the coordination between the extrinsic and intrinsic muscles were observed during the static task. Intermuscular coherence values generally decreased during the static task under assistance, but increased during the dynamic task (all p-values < 0.01). Additionally, a significant change in the task dynamics was induced by assistance only during static task. Our study showed that task type significantly affect coordination between the extrinsic and intrinsic hand muscles. During the static task, a lack of sensory information from musculotendons and joint receptors (more sensitive to changes in length/force) is postulated to have resulted in a neural decoupling between muscles and a consequent isolated modulation of the intrinsic muscle activity.     

The brain can eat: Establishing the existence of a central pattern generator for feeding in third instar larvae of Drosophila virilis and Drosophila melanogaster

To establish the existence of a central pattern generator for feeding in the larval central nervous system of two Drosophila species, the gross anatomy of feeding related muscles and their innervation is described, the motor units of the muscles identified and rhythmic motor output recorded from the isolated CNS. The cibarial dilator muscles that mediate food ingestion are innervated by the frontal nerve. Their motor pathway projects from the brain through the antennal nerves, the frontal connectives and the frontal nerve junction. The mouth hook elevator and depressor system is innervated by side branches of the maxillary nerve. The motor units of the two muscle groups differ in amplitude: the elevator is always activated by a small unit, the depressor by a large one. The dorsal protractors span the cephalopharyngeal skeleton and the body wall hence mediating an extension of the CPS. These muscles are innervated by the prothoracic accessory nerve. Rhythmic motor output produced by the isolated central nervous system can simultaneously be recorded from all three nerves. The temporal pattern of the identified motor units resembles the sequence of muscle contractions deduced from natural feeding behavior and is therefore considered as fictive feeding. Phase diagrams show an almost identical fictive feeding pattern is in both species.     

Fast drum strokes: Novel and convergent features of sonic muscle ultrastructure,innervation, and motor neuron organization in the pyramid butterflyfish (hemitaurichthys polylepis)

Sound production that is mediated by intrinsic or extrinsic swim bladder musculature has evolved multiple times in teleost fishes. Sonic muscles must contract rapidly and synchronously to compress the gas‐filled bladder with sufficient velocity to produce sound. Muscle modifications that may promote rapid contraction include small fiber diameter, elaborate sarcoplasmic reticulum (SR), triads at the A–I boundary, and cores of sarcoplasm. The diversity of innervation patterns indicate that sonic muscles have independently evolved from different trunk muscle precursors. The analysis of sonic motor pathways in distantly related fishes is required to determine the relationships between sonic muscle evolution and function in acoustic signaling. We examined the ultrastructure of sonic and adjacent hypaxial muscle fibers and the distribution of sonic motor neurons in the coral reef Pyramid Butterflyfish (Chaetodontidae: Hemitaurichthys polylepis) that produces sound by contraction of extrinsic sonic muscles near the anterior swim bladder. Relative to adjacent hypaxial fibers, sonic muscle fibers were sparsely arranged among the endomysium, smaller in cross‐section, had longer sarcomeres, a more elaborate SR, wider t‐tubules, and more radially arranged myofibrils. Both sonic and non‐sonic muscle fibers possessed triads at the Z‐line, lacked sarcoplasmic cores, and had mitochondria among the myofibrils and concentrated within the peripheral sarcoplasm. Sonic muscles of this derived eutelost possess features convergent with other distant vocal taxa (other euteleosts and non‐euteleosts): small fiber diameter, a well‐developed SR, and radial myofibrils. In contrast with some sonic fishes, however, Pyramid Butterflyfish sonic muscles lack sarcoplasmic cores and A–I triads. Retrograde nerve label experiments show that sonic muscle is innervated by central and ventrolateral motor neurons associated with spinal nerves 1–3. This restricted distribution of sonic motor neurons in the spinal cord differs from many euteleosts and likely reflects the embryological origin of sonic muscles from hypaxial trunk precursors rather than occipital somites. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Regulation of Jaw-specific Isoforms of Myosin-binding Protein-C and Tropomyosin in Regenerating Cat Temporalis Muscle Innervated by Limb Fast and Slow Motor Nerves

Cat jaw-closing muscles are a distinct muscle allotype characterized by the expression of masticatory-specific myofibrillar proteins. Transplantation studies showed that expression of masticatory myosin heavy chain (m-MyHC) is promoted by fast motor nerves, but suppressed by slow motor nerves. We investigated whether masticatory myosin-binding protein-C (m-MBP-C) and masticatory tropomyosin (m-Tm) are similarly regulated. Temporalis muscle strips were transplanted into limb muscle beds to allow innervation by fast or slow muscle nerve during regeneration. Regenerated muscles were examined postoperatively up to 168 days by peroxidase IHC using monoclonal antibodies to m-MyHC, m-MBP-C, and m-Tm. Regenerates in both muscle beds expressed fetal and slow MyHCs, m-MyHC, m-MBP-C, and m-Tm during the first 4 weeks. Longer-term regenerates innervated by fast nerve suppressed fetal and slow MyHCs, retaining m-MyHC, m-MBP-C, and m-Tm, whereas fibers innervated by slow nerve suppressed fetal MyHCs and the three masticatory-specific proteins, induced slow MyHC, and showed immunohistochemical characteristics of jaw-slow fibers. We concluded that expression of m-MBP-C and m-Tm is coregulated by m-MyHC and that neural impulses to limb slow muscle are capable of suppressing masticatory-specific proteins and to channel gene expression along the jaw-slow phenotype unique to jaw-closing muscle. (J Histochem Cytochem 58:989–1004, 2010)     

Myonic makeup of the muscles innervated by the vagus nerve

Histochemical investigation on succinic dehydrogenase activity and morphometric studies have demonstrated certain differences in the dog sublingual group of muscles. The thyreohyoid and sternohyoid muscles innervated by spinal nerves possess three types of myons differing in succinic dehydrogenase activity and in the area of transversal section. The cricothyreoid muscle and the superior pharyngeal constrictor obtaining their motor innervation from the vagus nerve are composed of unitypical muscular fibres with nearly the same areas of transversal section and high enzymic activity. The differences noted should be explained by different sources of motor innervation.     

Junctional acetylcholine receptor channel open time is not presynaptically regulated in developing muscle

The role of motor innervation in controlling the development of acetylcholine receptor (AChR) channel open time was tested by examining synaptic current durations in transplanted muscles of Xenopus tadpoles. The presumptive lower jaw region, which gives rise to the interhyoideus muscle, was transplanted to the tail, overlying the myotomal muscle cells. The transplanted muscles became innervated, presumably by spinal nerves which normally innervate myotomal muscle. Despite development in the presence of foreign innervation, synaptic currents in the transplanted interhyoideus were predominantly long in duration and resembled those in the normally innervated interhyoideus. They did not resemble those in the myotomal muscle, where synaptic currents are brief. The apparent lack of neural influence on development of AChR function in muscle contrasts with the evidence for presynaptic control of AChR open time in frog sympathetic ganglia. This may reflect a fundamental difference between nerve and muscle in the regulation of postsynaptic function.     

Muscles and nerves of the posterior abdomen and genitalia of male Periplaneta americana (L.) (Dictyoptera : Blattidae)

Segmental and intersegmental muscles of abdominal segments 7–10 are described for adult, male Periplaneta americana (L.) (Dictyoptera : Blattidae). Locations of extrinsic and intrinsic genitalic muscles are documented, and the actions of those associated with the right phallomere are hypothesized. Muscles of the 5 abdominal segments are innervated by branches from 5 pairs of segmental nerves and 3 pairs of transverse nerves. These stem from a terminal synganglion, formed during embryogenesis by fusion of neuromeres of abdominal segments 7–11. One pair of segmental nerves issues from each of the 5 neuromeres, and one pair of transverse nerves arises from neuromeres of abdominal segments 7–9. The nerves are traced to the muscles, integument, and reproductive glands, and their peripheral unions are characterized. Serial homologies of the nerves and muscles are proposed, and comparisons are made with neuromusculature of the female.     

Reanimation of the hemiparalytic tongue

Tongue hemiparesis is the inevitable result when the freshly severed 12th nerve is anastomosed to the trunk of a paralyzed 7th nerve in the technique commonly used by neurosurgeons, head and neck surgeons, otologists, and plastic surgeons to treat unilateral facial paralysis. This author has reactivated hemiparalytic tongues after research on cats. The technique has now been proved to be successful on two human beings. The reanimation is based on a simple Z-plasty of tongue muscle across the midline. Two principles are established: (1) placing a normal muscle in direct contact with a denervated muscle stimulates axons from the normal side to penetrate into the denervated side, eventually restoring function, and (2) transposition of a flap of muscle from the normal side containing extrinsic tongue muscles could provide a motor apparatus to activate the paralytic side. Biopsy slides taken from the paralyzed side of the cat tongues after 18 months showed sprouting of multiple nerves. Nerve sprouting can be found in human tongues 1 year after Z-plasties. The two patients who experienced atrophy and hemiparesis after the 12th-7th nerve hookup regained full range of tongue movements by 2 months and 4 months, respectively, demonstrating that with time, motor axons from the normal side innervated the atrophic muscle side to form new neuromotor junctions resulting in tongue movements. EMGs of the reanimated tongue showed normal activity in both sides of the tongue. Biopsies of the interface between the normal and former paralyzed side taken 1 year later showed nerves crossing the scar barrier. Apparently, the role of additional extrinsic muscle to the paralyzed side played a minor role.     

Homologies of the branchial arch muscles in Zacco platypus (Teleostei: Cypriniformes: Cyprinidae): Evidence from innervation pattern

Homologies of the branchial arch muscles in the cyprinid Zacco platypus are assessed based on their innervation. Muscles serving the first gill arch are innervated by branches of the glossopharyngeal (IX) nerve and those serving other arches by the vagal (X) nerve. Absence of the levator posterior is confirmed. Five pairs of muscles originating from the cranium and inserted onto the specialized 5th ceratobranchial, all unique to cyprinids, are innervated by the 4th branchial trunks of X, indicating that all pairs are derivatives of the sphincter oesophagi, involving reorganization from intrinsic to extrinsic elements. Homologies of some ventral branchial muscles are also discussed and the criteria for homology improved by clarifying the innervation pattern. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Different motor learning effects on excitability changes of motor cortex in muscle contraction state

Abstract

We aimed to investigate whether motor learning induces different excitability changes in the human motor cortex (M1) between two different muscle contraction states (before voluntary contraction [static] or during voluntary contraction [dynamic]). For the same, using motor evoked potentials (MEPs) obtained by transcranial magnetic stimulation (TMS), we compared excitability changes during these two states after pinch-grip motor skill learning. The participants performed a force output tracking task by pinch grip on a computer screen. TMS was applied prior to the pinch grip (static) and after initiation of voluntary contraction (dynamic). MEPs of the following muscles were recorded: first dorsal interosseous (FDI), thenar muscle (Thenar), flexor carpi radialis (FCR), and extensor carpi radialis (ECR) muscles. During both the states, motor skill training led to significant improvement of motor performance. During the static state, MEPs of the FDI muscle were significantly facilitated after motor learning; however, during the dynamic state, MEPs of the FDI, Thenar, and FCR muscles were significantly decreased. Based on the results of this study, we concluded that excitability changes in the human M1 are differentially influenced during different voluntary contraction states (static and dynamic) after motor learning.     

Synaptic competition and the persistence of polyneuronal innervation at frog neuromuscular junctions

Mechanisms governing the elimination of polyneuronal innervation were examined by correlating the morphology and physiology of competing nerve terminals at identified dually innervated neuromuscular junctions in sartorius muscles of adult frogs (Rana pipiens). Synaptic efficacy (endplate potential amplitude per unit nerve terminal length) was presumed to reflect the ability of a terminal to compete for synaptic space. The synaptic efficacies of two terminals at the same synaptic site were found to be surprisingly equal, with a median difference of 33%. Much more variation would be expected if dually innervated junctions were randomly innervated by pairs of terminals having the same range of synaptic efficacy as that found at singly innervated junctions in the same muscle. This finding supports the hypothesis that the weaker input is eliminated from dually innervated junctions when there is a large discrepancy in competitive efficacy, and that both inputs may persist if competitive efficacies are relatively equal. We also tested but failed to find support for the hypothesis that spatial proximity between competing terminals intensifies competition for synaptic space during synapse elimination.     

Anatomical partitioning of three multiarticular human muscles.

To examine neuromuscular partitioning within human muscles, the innervation patterns and muscle fiber architecture of the flexor carpi radialis (FCR), extensor carpi radialis longus (ECRL) and lateral gastrocnemius (LG) muscles were examined. Consistent patterns of innervation between specimens were found within each of the three muscles. The nerve to the FCR clearly innervates three major architectural divisions of the muscle. The ECRL is innervated by two different muscle nerves. Branches of these nerves innervate at least two distinct anatomical subvolumes. However, the subvolumes of the ECRL defined by muscle architecture are not totally congruent with those defined by the innervation pattern. In the LG, the single muscle nerve branches into two main divisions, and these subsequently divide into branches which supply the three heads. However, each head does not receive a completely private nerve. These results indicate that human muscles are partitioned in a manner roughly similar to the divisions of the same muscles in cats and rats, but with less congruency of architecture and innervation.     

Muscle type-specific myosin isoforms in crustacean muscles

Differential expression of multiple myosin heavy chain (MyHC) genes largely determines the diversity of critical physiological, histochemical, and enzymatic properties characteristic of skeletal muscle. Hypotheses to explain myofiber diversity range from intrinsic control of expression based on myoblast lineage to extrinsic control by innervation, hormones, and usage. The unique innervation and specialized function of crayfish (Procambarus clarkii) appendicular and abdominal musculature provide a model to test these hypotheses. The leg opener and superficial abdominal extensor muscles are innervated by tonic excitatory motoneurons. High resolution SDS-PAGE revealed that these two muscles express the same MyHC profile. In contrast, the deep abdominal extensor muscles, innervated by phasic motoneurons, express MyHC profiles different from the tonic profiles. The claw closer muscles are dually innervated by tonic and phasic motoneurons and a mixed phenotype was observed, albeit biased toward the phasic profile seen in the closer muscle. These results indicate that multiple MyHC isoforms are present in the crayfish and that differential expression is associated with diversity of muscle type and function.     

Musculature and innervation of the neck of the desert locust,Schistocerca gregaria (Forskål)

The innervation of each of the muscles involved in mediating head movement in the desert locust Schistocerca gregaria is described in detail. The number of motor neurones to each muscle and the neutral pathway and ganglion of origin of each are deduced from both histological and electrophysiological evidence. Only two of the muscles are, on histological evidence, innervated by as few as four different neurones, while several receive more than ten, and one at least 13. Individual muscles are shown physiologically to receive, in a few cases, as many as six different motor neurones. At least six muscles are innervated by motor neurones originating in more than one ganglion. One group of four muscles consisting in total of less than 100 muscle fibres receives more than 20 different motor neurones from three different ganglia through three or four different nerve roots. In these muscles, many single muscle fibres receive innervation from at least two different ganglia. It is concluded that the segmental nature of an insect muscle can not be deduced solely from a knowledge of the ganglion of origin of the motor innervation to that muscle. The innervation patterns that exist today must reflect past evolutionary development, but changes in the peripheral distribution of motor neurones, or migration of motor neurone cell bodies from one ganglion to another, or the development of additional motor neurones, or several of these factors together, must have formed a part of that development.     

Peptide-containing neurons intrinsic to the gut wall

Summary Nerve fibers containing substance P, VIP, enkephalin or somatostatin are numerous in the porcine gut wall. They are particularly numerous in the submucosal and myenteric plexuses where peptide-containing cell bodies are also observed. Peptide-containing nerve fibers occur also in the vagus nerves, suggesting that the gut receives an extrinsic supply of peptidergic nerves. The extrinsic contribution to the peptide-containing nerve supply of the gut wall has not yet been quantitatively assessed. In an attempt to clarify this question pigs were subjected to bilateral subdiaphragmatic vagotomy. Another group of animals was subjected to complete extrinsic denervation by autotransplantation of a jejunal segment. The pigs were killed at various time intervals after the operations; the longest time interval studied was four months. Following vagotomy the innervation pattern of the jejunum appeared completely unaffected. Following complete extrinsic denervation the adrenergic nerve fibers disappeared, while peptide-containing and acetylcholinesterase-positive nerve fibers remained apparently unaltered. This was confirmed chemically in the case of substance P.The motor activity of smooth muscle from the jejunum was studied in vitro. At low stimulation frequencies the smooth muscle from control jejunum responded by relaxation; upon cessation of stimulation a contraction occurred. With increasing stimulation frequencies the duration of the relaxation decreased; at high frequency stimulation only a contraction was recorded. In the autotransplant low frequency stimulation induced no or only a weak relaxation; high frequency stimulation induced contraction. After cholinergic and adrenergic blockade, the muscle responded with relaxation at all frequencies; the response was similar in innervated and denervated specimens. On the whole, the effects of extrinsic denervation on the motor activity of smooth muscle from porcine jejunum were minor, possibly reflecting the high degree of autonomy of the gut.     

Transneuronal induction of muscle atrophy in grasshoppers

Autotomy is a process in grasshoppers whereby one or both hindlimbs can be shed to escape a predator or can be abandoned if damaged. It occurs between the trochanter and the femur (second and third leg segments) and once lost, the legs never regenerate. Autotomy severs branches of the leg nerve (N5) but damages no muscles since none span the autotomy plane. We find, however, that undamaged muscles intrinsic to the thorax of grasshoppers, Barytettix psolus, atrophy to less than 15% of their normal mass after autotomy of a hindlimb. These muscles operate the coxa and trochanter (first and second leg segments) and are innervated by branches of nerves 3 and 4; nerve branches that are not damaged by autotomy. Atrophy is localized to the side and body segment where autotomy occurs. Atrophy is evident 7-10 days after loss of a limb, is complete by about 30 days, and follows a similar time course whether induced in young adult, or sexually mature grasshoppers. During autotomy, leg nerve 5 is served distal to the trochanter, the thoracic muscles lose their normal static and dynamic load, and these muscles are subsequently no longer used to support the weight of the insect during posture and locomotion. Experimental loading and unloading of the affected muscles, and cutting of nerves indicated that it is the severing of leg nerve 5 during autotomy that transneuronally induces muscle atrophy.     

Scanning and freeze-fracture study of larval nerves and neuromuscular junctions in Manduca sexta

The nerves and nerve terminals to tonic larval muscle fibers in third and fifth instar caterpillars were studied to compare them with those formed by the same motor neurons on phasic flight muscles in adult moths. Scanning micrographs showed a primary nerve branch running the length of each fiber, with secondary nerve branches extending from it at intervals. There was a great deal of variability in both the length of the branches and the distance from the nerve at which the neuromuscular junctions were formed. The rapid increase in muscle fiber size during larval development may be responsible for this variability. The nerves and junctions were often found to be obscure by overlying fibroblasts and tracheoblasts or entering the deep muscle clefts. Those examined were similar in appearance to the adult junctions formed by the same neurons, although some may have formed single branches instead of y-shapes. The membrane specializations of the synapse seen in freeze-fractured specimens were similar to those of the adult junction. However, the overall shape of the nerve terminal within the junction differed. The larval nerve terminals appeared varicose instead of having a uniform diameter. The spacing of the nerve plaques varied, in contrast with the relatively straight alignment and even spacing of plaques found in adult junctions. Such differences could result from an interaction between the motor neuron and the two different types of muscle fiber that it innervates, an intrinsic change in the motor neurons themselves that occurs with metamorphosis, or a plastic functional response that occurs as a result of the different types of motor patterns that are used in the two stages.     

The effect of two episodes of denervation and reinnervation on skeletal muscle contractile function.

Sensory or motor "baby-sitting" has been proposed as a clinical strategy to preserve muscle integrity if motion-specific axons must regenerate over a long distance to reach denervated target muscles. Denervated muscles are innervated temporarily by using axons from nearby sensory or motor nerves. After motion specific motor axons have reached the target, the baby-sitter nerve is severed and motion-specific axons are directed to the target. Although this strategy minimizes denervation time, the requisite second episode of denervation and reinnervation might be deleterious to muscle contractile function. This study was designed to test the hypothesis that two sequential episodes of skeletal muscle denervation and reinnervation result in greater force and power deficits than a single peripheral nerve injury and repair. Adult Lewis rats underwent either transection and epineurial repair or sham exposure of the left peroneal nerve. After a 4-month recovery period, the contractile properties of the extensor digitorum longus muscle of the sham exposure group (control, n = 9) and one of the nerve division and repair groups (repair group 1, n = 9) were evaluated with measurements of the maximum tetanic isometric force, peak power, and maximal sustained power. A third group of rats underwent a second cycle of nerve division and repair (repair group 2, n = 9) at this same time point. Four months postoperatively, contractile properties of the extensor digitorum longus muscles were evaluated. Maximum tetanic isometric force and peak power were significantly reduced in repair group 2 rats as compared with repair group 1 and control rats. Maximal sustained power was not significantly different between the groups. These data support our working hypothesis that skeletal muscle contractile function is adversely affected by two cycles of denervation and reinnervation as compared with a single episode of nerve division and repair.     

The pattern of innervation in serially duplicated axolotl limbs: further evidence for the existence of local pathway cues?

The innervation of the biceps muscle was examined in regenerated and vitamin A-induced serially duplicated axolotl forelimbs using retrograde transport of horseradish peroxidase. The regenerated biceps muscle becomes innervated by motor neurones in the same position in the spinal cord as the normal biceps motor pool. In previous experiments in which the innervation of a second copy of a proximal limb muscle was examined in serially duplicated limbs (Stephens, Holder & Maden, 1985), the duplicate muscle was found to become innervated by motor neurones that would normally have innervated distal muscles. In the present study, the innervation of the second copy of biceps was examined under conditions designed to encourage nerve sprouting from 'correct' biceps axons. Following either partial limb denervation or denervation coupled with removal of the proximal biceps, the second copy of the muscle was still innervated by inappropriate motor neurones, which again would normally innervate distal limb muscles. These results are interpreted as evidence for the necessity for an appropriate local environment for axonal growth to allow reformation of a correct pattern of motor innervation in the regenerated limb.