Determinants of directional specificity in the regeneration of lamprey spinal axons

Mackler, SA; Yin, Hsiang‐Shu; Selzer, ME

doi:10.1523/jneurosci.06-06-01814.1986

Cited by 47 publications

(37 citation statements)

References 23 publications

(29 reference statements)

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“…Animals in which hemisection was judged to be incomplete or to extend far beyond the midline at the time of surgery were discarded, but slight overhemisection was accepted and even presumed. To block regeneration of transected reticulospinal axons, 5 mm of spinal cord caudal to the transection was excised, leaving a large gap through which transected axons were incapable of regenerating (Mackler et al, 1986). Successful regeneration of reticulospinal axons requires the presence of glial elements in the lesion site (Lurie and Selzer, 1991b).…”

Section: Methodsmentioning

confidence: 99%

“…Reticulospinal axons of larval and adult lampreys regenerate selectively in their correct directions across complete transections of the spinal cord Mackler et al, 1986;Lurie and Selzer, 1991a). By 10 weeks after spinal transection, larval lampreys recover behavioral functions (Rovainen, 1976;Selzer, 1978) that are mediated by the formation of synapses with appropriate neurons distal to the site of injury (Mackler and Selzer, 1987).…”

Section: Heterogeneity Of Cns Axon Regenerationmentioning

confidence: 99%

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Recovery of Neurofilament Expression Selectively in Regenerating Reticulospinal Neurons

et al. 1997

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During regeneration of lamprey spinal axons, growth cones lack filopodia and lamellipodia, contain little actin, and elongate much more slowly than do typical growth cones of embryonic neurons. Moreover, these regenerating growth cones are densely packed with neurofilaments (NFs). Therefore, after spinal hemisection the time course of changes in NF mRNA expression was correlated with the probability of regeneration for each of 18 identified pairs of reticulospinal neurons and 12 cytoarchitectonic groups of spinal projecting neurons. During the first 4 weeks after operation, NF message levels were reduced dramatically in all axotomized reticulospinal neurons, on the basis of semiquantitative in situ hybridization for the single lamprey NF subunit (NF-180). Thereafter, NF expression returned toward normal in neurons whose axons normally regenerate beyond the transection but remained depressed in poorly regenerating neurons. The recovery of NF expression in good regenerators was independent of axon growth across the lesion, because excision of a segment of spinal cord caudal to the transection site blocked regeneration but did not prevent the return of NF-180 mRNA. The early decrease in NF mRNA expression was not accompanied by a reduction in NF protein content. Thus the axotomy-induced loss of most of the axonal volume resulted in a reduced demand for NF rather than a reduction in volume-specific NF synthesis. We conclude that the secondary upregulation of NF message during axonal regeneration in the lamprey CNS may be part of an intrinsic growth program executed only in neurons with a strong propensity for regeneration.

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Section: Methodsmentioning

confidence: 99%

Section: Heterogeneity Of Cns Axon Regenerationmentioning

confidence: 99%

Recovery of Neurofilament Expression Selectively in Regenerating Reticulospinal Neurons

et al. 1997

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“…Micro-electrodes filled with 4-8 % (w/v) horseradish peroxidase (HRP; Yin & Selzer, 1983) (Yin, Mackler & Selzer, 1984;Mackler et al 1986). The experimental design is illustrated in Fig.…”

Section: Methodsmentioning

confidence: 99%

“…were selected. Previous experiments have shown that lamprey spinal axons regenerate preferentially in their normal rostral-caudal direction and on the correct side of the spinal cord Mackler et al 1986). The dendritic trees of g.i.s span the entire width of the spinal cord.…”

Section: Selectivity Of Synapse Formation By Regenerating Lamprey Axonsmentioning

confidence: 99%

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Specificity of synaptic regeneration in the spinal cord of the larval sea lamprey.

Mackler

Selzer

1987

The Journal of Physiology

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SUMMARY1. Pairs of central neurones in large larval sea lampreys were impaled with micro-electrodes and studied for synaptic connexions in both unoperated control animals and animals which had recovered from complete spinal transection. Two identified classes of neurones served as post-synaptic targets: giant interneurones (g.i.s) and lateral cells (l.c.s). Several identified neurone types were tested as potential sources of presynaptic input.2. When synaptic potentials had short, fixed latencies they also persisted during activation of the presynaptic cell at 3 3-33 3 Hz and were not eliminated after addition of lamprey saline containing high (20 mM) Ca2+. These presumably represented monosynaptic connexions. Variable-latency responses were eliminated by faster rates of stimulation of the presynaptic cell and were mediated via polysynaptic pathways.3. In control animals, g.i.s received monosynaptic input from more caudal g.i.s in fourteen of thirty-two tested cell pairs. These excitatory post-synaptic potentials (e.p.s.p.s) were composite electrochemical responses. The amplitudes of the earlier electrical component averaged 1-66 + 0-24 mV -(mean+ s.E. of mean) and the amplitude of the later chemical component averaged 0-79 ± 0 05 mV.4. In operated larvae, eight of forty-seven g.i.-g.i. pairs separated by the transection scar were connected by monosynaptic composite e.p.s.p.s. In these pairs the electrical component averaged 0-84 + 0-17 mV (P < 0 05 vs. control) and the chemical component averaged 1 56 + 0 40 mV. The average conduction velocity between these cells was less than that in control g.i.-g.i. pairs (0-93 + 0-11 vs. 1-61 + 0-25 m/s; P<0-01).5. The l.c.s showed monosynaptic e.p.s.p.s after activation of a subset of the bulbar Muller neurones (B2<) in seven of twelve pairs. In behaviourally recovered larvae three of twenty-two similar pairs separated by the transection scar were also connected via monosynaptic e.p.s.p.s. The average conduction velocity between these experimental neurones was also less than that in control bulbar-l.c. pairs (1-03+0-03vs. 1-58+0-09 m/s; P < 0-001).6. Several types of neurones were either infrequently linked or never connected to g.i.s or to l.c.s in control larvae. In animals which had recovered from a spinal S. A. MACKLER AND M. E. SELZER transection, no synaptic connexions were found from such neurones on to g.i.s or l.c.s respectively, in 124 tested cell pairs. In addition, dorsal cells (intraspinal primary sensory neurones) received no synaptic input upon stimulation of the spinal cord before or after transection.7. These findings indicate that regenerating spinal axons in the larval sea lamprey form functioning synapses directly onto neurones positioned within 8 mm distal to the healed transection scar. These axons appear to exhibit selectivity in their choice of synaptic targets.

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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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Determinants of directional specificity in the regeneration of lamprey spinal axons

Cited by 47 publications

References 23 publications

Recovery of Neurofilament Expression Selectively in Regenerating Reticulospinal Neurons

Recovery of Neurofilament Expression Selectively in Regenerating Reticulospinal Neurons

Specificity of synaptic regeneration in the spinal cord of the larval sea lamprey.

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

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