Intrinsic and extrinsic factors influencing properties and growth patterns of identified leech neurons in culture

Acklin, SE; Nicholls, J. G.

doi:10.1523/jneurosci.10-04-01082.1990

Cited by 45 publications

(25 citation statements)

References 22 publications

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“…Additional techniques for cell manipulations will be required in further investigations of this notion. However, our result is consistent with previous observations in dissociated cultures of mammalian hippocampal and cortical neurons (Kriegstein and Dichter, 1983;Bartlett and Banker, 1984) and of identified invertebrate neurons (Hadley et al, 1985;Acklin and Nicholls, 1990) that intrinsic factors play an important role in determining the basic features of nerve cells such as the number of primary projections.…”

Section: B Multipolarsupporting

confidence: 93%

“…The general morphology, such as arborization patterns of DrosopIzila nerve cells, are rather stable in culture (Kim and Wu. 1987) as has been shown in other organisms (Bray, Bunge, and Chapman, 1987;Acklin and Nicholls, 1990). Once primary neurites are differentiated, further development of Drosophilu neurons in culture involves mainly elaboration of primary processes (Kim and Wu.…”

Section: Introductionmentioning

confidence: 71%

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Distinctions in growth cone morphology and motility between monopolar and multipolar neurons in Drosophila CNS cultures

Kim

1991

J. Neurobiol.

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Growth cones play a central role in determining neurite extension, pathfinding and branching, and in establishing synaptic connections. This paper describes an initial characterization of growth cone morphology and behavior in dissociated larval central nervous system (CNS) cultures of Drosophila. Contrast-enhanced video images of growth cones in monopolar and multipolar neurons were characterized by employing morphometric parameters such as the number and length of filopodia, and the area and roundness of the lamellipodia. Behavior of growth cones was analyzed by a motility index and boundary flow plots originally devised for measuring motility in other cellular systems. We found that separate CNS regions yielded cultures of different major cell types with distinct neuritic patterns that could be correlated with the morphology and motility of the associated growth cones. Monopolar neurons were the major cell type in brain cultures, whereas multipolar neurons were predominant in ventral ganglion cultures. Moreover, the growth cones of monopolar neurons, which are likely to be associated with the axonal processes, differed from those of multipolar neurons, which might be related to dendritic terminals. Growth cones in monopolar neurons had larger lamellipodia of less erratic shape accompanied by fewer and shorter filopodia, and, when active, displayed much higher motility and less directionality in motion. Alternatively, these morphological and behavioral distinctions between monopolar and multipolar neurons may result from intrinsic differences in membrane adhesion and intracellular transport properties.

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Section: B Multipolarsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 71%

Distinctions in growth cone morphology and motility between monopolar and multipolar neurons in Drosophila CNS cultures

Kim

1991

J. Neurobiol.

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“…While Our present experiments do not rule out intrinsically controlled recapitulation of branching pattern, these peripheral axons had aligned longitudinally in a trajectory that would direct them toward the cut ends of intact heart tube several segments away. Other leech neurons have been shown to be capable of recapitulating major branch points in vitro (Acklin and Nicholls, 1990) and HEs may well be similarly restricted to generate a particular type or number of branch points. Our present results are also consistent with the idea that the intact heart muscle exerts a trophic or tropic influence over HE growth cones from some distance.…”

mentioning

confidence: 99%

Sprouting and connectivity of embryonic leech heart excitor (HE) motor neurons in the absence of their peripheral target

Jellies

Kopp

1995

Invertebrate Neuroscience

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The rhythmic pumping of the hearts in the medicinal leech, Hirudo medicinalis, is neurogenic and mediated by a defined circuit involving identified interneurons in a central pattern generator (CPG) and segmentally iterated motor neurons that drive the heart muscle. During early embryogenesis, presumptive heart excitor (HE) motor neurons extend many axon branches into the body wall; they later innervate the heart while retracting the supernumerary peripheral axons, and only much later in development receive synaptic input from the central pattern generator (Jellies, Kopp and Bledsoe (1992) J. Exp. Biol., 170, 71-92.). In this study, HE motor neurons were deprived of an early interaction with the heart by surgical ablation of a circumscribed portion of body wall including the heart primordium. Anatomical and electrophysiological data were obtained using intracellular techniques to examine the hypothesis that peripheral interactions with the developing heart provide instructive cues for the final differentiation of these neurons. Target-deprived HE motor neurons continued to extend multiple axons in ventral, lateral and dorsal body wall throughout late embryonic and into postembryonic stages and they extended anomalous axons within the CNS. This resembles the early embryonic growth of HE motor neurons before heart tube differentiation. Furthermore, HE motor neurons deprived of heart contact exhibited tonic activity similar to the situation during early development before they are contacted by the CPG interneurons. In contrast, sham-operated and contralateral HE motor neurons oscillated normally. These results suggest that heart tube contact is specifically required for at least some aspects of HE development and provide a framework in which to identify cell-cell interactions that are involved in matching neurons and targets to generate behaviorally relevant neural circuits.

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“…The same cells reproduce these patterns in culture. Disruption of the microtubular array does not affect the ability of the cell to regrow in a bipolar fashion ( Acklin and Nicholls, 1990). These results have shown that substrate molecules are of critical importance for inducing the growth of leech nerve cells, and that it is actually the local interaction between the substrate and the neurites that determines the pattern of outgrowth.…”

Section: Growth Of Leech Nerve Cells In Culture Depends On the Substratementioning

confidence: 78%

The role of matrix molecules in regeneration of leech CNS

Masuda-Nakagawa

Wiedemann

1992

J. Neurobiol.

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Extracellular matrix (ECM) molecules extracted from the leech central nervous system (CNS) provide substrates that induce extensive growth of processes of identified leech nerve cells in culture. Two ECM molecules, laminin and tenascin, have been identified. The laminin-like molecule has been purified and shown to be a cross-shaped molecule similar to vertebrate laminin with subunits of 340, 220, 180, and 160 kD. Purified laminin as a substrate induces rapid outgrowth of Retzius (R) and Anterior Pagoda (AP) cells in culture. The tenascin molecule has been partially purified. In electronmicrographs, leech tenascin, like vertebrate tenascin, has six arms of equal size joined in a central globule. Highly enriched fractions of leech tenascin induce rapid and extensive outgrowth of Retzius and AP cells in culture. Substrate molecules not only induce outgrowth of processes but also affect the growth patterns of individual nerve cells. Neurites are straight with few branches in laminin, but curved with profuse branches on tenascin. During regeneration of the CNS in the animal, laminin appears at new sites associated with growth cones. The appearance of laminin correlates with the accumulation of microglial cells. Thus, ECM molecules with growth-promoting activity for leech nerve cells in vitro appear to be involved in inducing regeneration and allowing the neurites to reconnect with former targets.

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Intrinsic and extrinsic factors influencing properties and growth patterns of identified leech neurons in culture

Cited by 45 publications

References 22 publications

Distinctions in growth cone morphology and motility between monopolar and multipolar neurons in Drosophila CNS cultures

Distinctions in growth cone morphology and motility between monopolar and multipolar neurons in Drosophila CNS cultures

Sprouting and connectivity of embryonic leech heart excitor (HE) motor neurons in the absence of their peripheral target

The role of matrix molecules in regeneration of leech CNS

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