Regeneration of an identifiable motoneuron in the crayfish. II. Patterns of reconnection and synaptic strength established in the presence of an extra nerve

Hunt, William P.; Vélez, Samuel J.

doi:10.1002/neu.480200805

Cited by 11 publications

(3 citation statements)

References 20 publications

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“…At later stages of regeneration these inappropriate axonal branches become eliminated until this muscle is again innervated by its single motoneuron (Denburg, 1982). Formation and subsequent elimination of redundant connections were also shown in crayfish neuromuscular regeneration (Goransson et aI., 1988;Hunt and Velez, 1989). Formation of the transient novel connections between regenerating neurons was observed in molluscs Cohan et al, 1987).…”

Section: Formation and Elimination Of Abundant Connections During Motmentioning

confidence: 90%

Regeneration of central and peripheral synaptic connections in the locomotor system of the pteropod molluscClione limacina

Panchin

Zelenin

Popova

1997

Invertebrate Neuroscience

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The neural network underlying rhythmic wing movements in the mollusc CIione limacina is well-studied. Two different groups of motoneurons innervate two distinct groups of wing muscles. The locomotor rhythm generated in the left and right pedal ganglia is synchronized by interneurons. When the axons of the locomotor motoneurons are crushed, numerous fine neurites sprout towards the denervated muscles and reach them in 8-15 days. At this stage motoneurons project to and synapse on not only correct but equally incorrect muscle targets. After 2 weeks of regeneration the number of incorrect neurites and synaptic connections begins to decrease and following 1.5-2 months all incorrect connections are eliminated, incorrect axons are withdrawn and the behavioral deficit is compensated. In this study the regeneration of intemeurons and the growth profiles of inter-and motoneurons were also studied in vitro. Two individually isolated pedal ganglia were co-cultured in three different configurations: a) the wing nerve stump from one ganglion was fixed against the commissural stump from another ganglion; b) the wing nerve stumps were fixed against each other; c) the commissural stumps were fixed against each other. Under the above experimental conditions we found that the interneurons were able to cross only the contact between two commissural stumps, and in this case found their original targets, restored correct connections and synchronized the rhythm in two pedal ganglia. In contrast, motoneurons were able to cross all types of contacts.

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Section: Formation and Elimination Of Abundant Connections During Motmentioning

confidence: 90%

Regeneration of central and peripheral synaptic connections in the locomotor system of the pteropod molluscClione limacina

Panchin

Zelenin

Popova

1997

Invertebrate Neuroscience

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“…The possibility of hyperinnervation of intact muscles needs to be explored. Some authors suggest that a normally innervated muscle can not be subjected to further innervation (Frank and Jansen, 1976; Robbins et al, 1977; Slack, 1978) but some show that the hyperinnervation is possible (Bixby and Van Essen, 1979; Hunt and Velez, 1982, 1989). As demonstrated in the present study, new innervation occurred in the wing muscles and was superimposed on their initial innervation, when the contralateral motoneurons were induced to sprout.…”

Section: Discussionmentioning

confidence: 99%

Projection pattern and target selection ofClione limacina motoneurons sprouting within an intact environment

Zelenin

Panchin

2000

J. Comp. Neurol.

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In the pteropod mollusc Clione limacina, two groups of locomotor motoneurons, located in the pedal ganglion, innervate the dorsal and ventral muscle layers of the ipsilateral wing through the wing nerve. Separate branches of this nerve go either only to the dorsal muscle layer or only to the ventral one. In the present study, growth of novel neurites of the wing motoneurons was induced by cutting the wing nerve. In addition, all other peripheral nerves and connectives of the pedal ganglion were cut, except for the pedal commissure to the contralateral pedal ganglion. Thus, the neurites were allowed to grow only towards the contralateral pedal ganglion. We have found that the novel neurites, entering the contralateral pedal ganglion, were capable of growing everywhere inside the central nervous system (CNS) and into any peripheral nerve. However, they preferred the wing nerve. This finding suggests that the preference is caused by the guiding cues in the wing nerve or the attractive influence of the wing muscles. Because the contralateral pedal ganglion and nerves were left intact, the growth direction of the new neurites could be determined only by factors permanently existing in the CNS, rather than induced by nerve injury or muscle denervation. Within the wing nerve, the neurites could not discriminate between the nerve branches going to the dorsal and ventral muscle layers. They formed synapses on muscles of both layers, despite the fact that the muscles were innervated by their own motoneurons.

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“…After the SFM nerve was transected and the original innervation had degenerated, the regenerating proximal ends of the motor axons formed a pattern of synaptic connections similar to the original (Ely and Velez, 1982). Such a high degree of specificity of synaptic reconnections occurred despite drastic manipulation of the muscle (Hunt and Velez, 1982;Clement et al, 1983;Hunt and Velez 1989a) or nerve (Goransson et al 1988;Worden et al 1988;Hunt and Velez 1989b).…”

Section: Introductionmentioning

confidence: 93%

Allotransplanted nerves regenerate inhibitory synapses on a crayfish muscle: Possible postsynaptic specification

2002

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Donor nerves of different origins, when transplanted onto a previously denervated adult crayfish abdominal superficial flexor muscle (SFM), regenerate excitatory synaptic connections. Here we report that an inhibitory axon in these nerves also regenerates synaptic connections based on observation of nerve terminals with irregular to elliptically shaped synaptic vesicles characteristic of the inhibitory axon in aldehyde fixed tissue. Inhibitory terminals were found at reinnervated sites in all 12 allotransplanted-SFMs, underscoring the fact that the inhibitory axon regenerates just as reliably as the excitatory axons. At sites with degenerating nerve terminals and at sparsely reinnervated sites, we observe densely stained membranes, reminiscent of postsynaptic membranes, but occurring as paired, opposing membranes, extending between extracellular channels of the subsynaptic reticulum. These structures are not found at richly innervated sites in allotransplanted SFMs, in control SFMs, or at several other crustacean muscles. Although their identity is unknown, they are likely to be remnant postsynaptic membranes that become paired with collapse of degenerated nerve terminals of excitatory and inhibitory axons. Because these two axons have uniquely different receptor channels and intramembrane structure, their remnant postsynaptic membranes may therefore attract regenerating nerve terminals to form synaptic contacts selectively by excitatory or inhibitory axons, resulting in postsynaptic specification.

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Regeneration of an identifiable motoneuron in the crayfish. II. Patterns of reconnection and synaptic strength established in the presence of an extra nerve

Cited by 11 publications

References 20 publications

Regeneration of central and peripheral synaptic connections in the locomotor system of the pteropod molluscClione limacina

Regeneration of central and peripheral synaptic connections in the locomotor system of the pteropod molluscClione limacina

Projection pattern and target selection ofClione limacina motoneurons sprouting within an intact environment

Allotransplanted nerves regenerate inhibitory synapses on a crayfish muscle: Possible postsynaptic specification

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