Distribution and morphology of inhibitory innervation in crayfish ( Procambarus clarkii ) limb and abdominal muscles

Msghina, Mussie; Atwood, H. L.

doi:10.1007/s004410050913

Cited by 11 publications

(12 citation statements)

References 33 publications

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“…These findings are in agreement with the observations of Msghina and Atwood (1997), who compared the phasic and tonic inhibitory innervation in disparate limb and abdominal muscles. Our quantitative findings in a unified functional system, that of the deep and superficial abdominal extensor muscles, supports the conclusion that structural differences relate specifically to the functional class (phasic vs. tonic) of muscle that the axons innervate.…”

Section: Discussionsupporting

confidence: 93%

Dichotomy in phasic‐tonic neuromuscular structure of crayfish inhibitory axons

Kirk

Meyer

Govind

2001

J of Comparative Neurology

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Crustacean muscles are unique in their innervation by both excitatory and inhibitory neurons; therefore, they exhibit polyneuronal and multiterminal innervation. Because excitatory motoneurons are broadly divided into phasic and tonic types, we hypothesized that inhibitory neurons would follow a similar dichotomy. The abdominal extensor muscles in crayfish are separated into parallel deep and superficial bundles; the former has fast muscle fibers innervated by phasic excitatory motoneurons, and the latter has slow fibers supplied by tonic excitatory motoneurons. Each muscle also is innervated by a single, separate inhibitory neuron that uses gamma-aminobutyric acid (GABA) as the inhibitory neurotransmitter. The pattern of axonal branching by the separate inhibitory axons in phasic and tonic abdominal extensor muscles was visualized with confocal microscopy in preparations labeled for GABA-like immunoreactivity. Initial observations indicated that the phasic muscle was covered by extensive GABAergic, filiform axon terminals, whereas innervation of the tonic muscle was comprised of more localized and varicose terminals. With quantitative analyses, we found that the phasic axon has a more highly branched nature than the tonic in first- and second-order branches. The phasic axon branches also were significantly longer than the tonic branches in the second- and third-order branches. Synaptic varicosities in the phasic branches were smaller and less frequent than those in the tonic branches. The fine structure of the inhibitory nerve terminals near synaptic contacts examined with thin-serial-section electron microscopy revealed distinct differences between the phasic system and the tonic system. The phasic terminals were smaller in cross-sectional area than the tonic terminals, and they had smaller synapses and fewer mitochondria. The presynaptic active zone dense bodies were similar in length and number between phasic and tonic synapses. However, their number per synaptic area was two-fold higher in phasic synapses compared with tonic synapses because of the smaller size of the phasic synapses. Thus, within the same neuromuscular system, inhibitory synaptic terminals revealed unique phasic and tonic identities similar to those observed for the excitatory axons.

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Section: Discussionsupporting

confidence: 93%

Dichotomy in phasic‐tonic neuromuscular structure of crayfish inhibitory axons

Kirk

Meyer

Govind

2001

J of Comparative Neurology

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“…Specifically, we report here that a majority of the lobster neuromuscular synapses have no associated dense bars, and that these lobster synapses have many fewer dense bars, overall, than have been reported for synapses on the crayfish dactyl opener muscle. In addition, whereas previous studies have reported that excitatory and inhibitory innervation sites on the crayfish dactyl opener muscle are co-localized (Govind et al 1994(Govind et al , 1995aCooper et al 1996a;Msghina and Atwood 1997), we have observed relatively large (~20 μm) regions in which inhibitory terminals are present, but excitatory terminals are absent, in lobster dactyl opener. These morphological differences are likely to have important implications for the interpretation of physiological data recorded from neuromuscular synapses in the dactyl opener of lobster.…”

Section: Introductioncontrasting

confidence: 73%

Neuromuscular synapses on the dactyl opener muscle of the lobster Homarus americanus

2006

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The crustacean dactyl opener neuromuscular system has been studied extensively as a model system that exhibits several forms of synaptic plasticity. We report the ultrastructural features of the synapses on dactyl opener of the lobster (Homarus americanus) as determined by examination of serial thin sections. Several innervation sites supplied by an inhibitory motoneuron have been observed without nearby excitatory innervation, indicating that excitatory and inhibitory inputs to the muscle are not always closely matched. The ultrastructural features of the lobster synapses are generally similar to those described previously for the homologous crayfish muscle, with one major distinction: few dense bars are seen at the presynaptic membranes of these lobster synapses. The majority of the lobster neuromuscular synapses lack dense bars altogether, and the mean number of dense bars per synapse is relatively low. In view of the finding that the physiology of the lobster dactyl opener synapses is similar to that reported for crayfish, these ultrastructural observations suggest that the structural complexity of the synapses may not be a critical factor determining synaptic plasticity.

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“…2B and D). This is similar to synaptotagmin labeling in crayfish motor neurons, where the protein is distributed in nerve terminals of excitatory and inhibitory motor neurons (Cooper et al, 1995;Msghina and Atwood, 1997). The Ha-CalpM staining pattern was not correlated with claw type (cutter vs. crusher) or with stage in the molt cycle (premolt, postmolt, or intermolt).…”

Section: Discussionmentioning

confidence: 55%

Muscle-specific calpain is localized in regions near motor endplates in differentiating lobster claw muscles

Medler¹,

Chang²,

Mykles³

2007

Comparative Biochemistry and Physiology Part A: Molecular &

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Calpains are Ca 2+ -dependent proteinases that mediate protein turnover in crustacean skeletal muscles. We used an antibody directed against lobster muscle-specific calpain (Ha-CalpM) to examine its distribution in differentiating juvenile lobster claw muscles. These muscles are comprised of both fast and slow fibers early in development, but become specialized into predominantly fast or exclusively slow muscles in adults. The transition into adult muscle types requires that myofibrillar proteins specific for fast or slow muscles to be selectively removed and replaced by the appropriate proteins. Using immunohistochemistry, we observed a distinct staining pattern where staining was preferentially localized in the fiber periphery along one side of the fiber. Immunolabeling with an antibody directed against synaptotagmin revealed that the calpain staining was greatest in the cytoplasm adjacent to synaptic terminals. In complementary analyses, we used sequence-specific primers with real-time PCR to quantify the levels of Ha-CalpM in whole juvenile claw muscles. These expression levels were not significantly different between cutter and crusher claws, but were positively correlated with the expression of fast myosin heavy chain. The anatomical localization of Ha-CalpM near motor endplates, coupled with the correlation with fast myofibrillar gene expression, suggests a role for this intracellular proteinase in fiber type switching.

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Distribution and morphology of inhibitory innervation in crayfish ( Procambarus clarkii ) limb and abdominal muscles

Cited by 11 publications

References 33 publications

Dichotomy in phasic‐tonic neuromuscular structure of crayfish inhibitory axons

Dichotomy in phasic‐tonic neuromuscular structure of crayfish inhibitory axons

Neuromuscular synapses on the dactyl opener muscle of the lobster Homarus americanus

Muscle-specific calpain is localized in regions near motor endplates in differentiating lobster claw muscles

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