Regeneration of an identified central neuron in the cricket. I. Control of sprouting from soma, dendrites, and axon

Abstract

When the axon of the medial giant interneuron (MGI) of the cricket is axotomized close to the cell body, the normally stable, characteristic dendritic arborization is induced to sprout supernumerary neurites. The origin of the induced dendritic sprouts is not random; they emerge preferentially from the dendritic tips and branches close to the exit of the axon from the terminal ganglion. If any growth also occurred from the axon, there was a reciprocal relationship between the extent of dendritic and axonal sprouting. On the other hand, axotomy distant to the cell body induces sprouting only from the axon and does not alter the dendritic structure of the MGI.After crushing the ventral nerve cord distant to the cell body, the MGI sprouted neurites from the proximal axonal stump which crossed the site of lesion and continued growing within the distal cord. After a distant cut of the cord, however, the axonal neurites formed a neuroma in the proximal cord stump at the site of lesion and stopped elongating after 1 month. At this time, supernumerary sprouts first began to emerge from the normally smooth, rounded contours of the cell body.Based on these observations, we propose that axotomized neurons produce membrane at a constant rate. This newly synthesized membrane is preferentially inserted into neurites emerging from the proximal axonal stump. When axonal neurites stop growing in a neuroma following a distant cut, then this new membrane appears as supernumerary neurites from the soma. After a close cut, the axon often dies back into the ganglion and appears unable to receive the full complement of sprouting membrane. In such cases, the balance of the newly synthesized membrane is inserted into the dendrites and the characteristic structure of the arborization is significantly altered.Differential growth in discrete regions of a developing neuron eventually results in a fully differentiated nerve cell with three morphological compartments: the soma, the dendrites, and the axon. This structural specialization may arise during development from a selective distribution pattern of specific membrane components characteristic of each neuronal compartment. The distinct structural and functional properties that emerge in each compartment during development are stabilized and maintained to yield the mature neuron. ' Axotomy can be employed to study the insertion of newly synthesized membrane associated with the induced regenerative growth. In such an experimental framework, a mature, fully developed neuron is challenged by partial removal of a specific morphological compartment, namely, its axon. To restore its fully differentiated state, an injured neuron must specifically initiate axonal growth while retaining the mature properties of the undamaged dendrites and cell body. Sprouting induced by axotomy therefore provides a model system for studying the mechanisms controlling both regional growth and stabilization of structure and function in a single neuron.We have chosen to investigate regeneration of an injure...

Neuronal plasticity in the adult invertebrate nervous system

“…Axotomy of these monopolar neurons close to the cell body, however, resulted in profuse sprouting from dendritic arbors and soma in addition to the proximal axonal stump (Fig. 1); (Roederer and Cohen, 1983). The total extent of neurite outgrowth per cell was found to be similar regardless of the site(s) of origin.…”

Microtubule destabilization and neurofilament phosphorylation precede dendritic sprouting after close axotomy of lamprey central neurons.

“…(1)(2)(3)(4)(5)(6)(7)(8)], some of which are probably important preliminaries to axonal regeneration. Most cellular consequences of axotomy are more marked after axotomy close to the soma than after more distant lesions (1).…”

“…Most cellular consequences of axotomy are more marked after axotomy close to the soma than after more distant lesions (1). "Close" axotomy has also been shown in several systems to cause a fundamental cellular change that does not occur at all after distant axotomy-i.e., a loss of the ability to regenerate the axon specifically from the axon stump, resulting in axonal regeneration from the dendritic tips as well as (or instead of) from the axon stump in a number of systems (6,(9)(10)(11). This loss of normal cellular polarity allows one to ask what the mechanisms are that control the site of axonal regeneration within the cell and also permits one to study the earliest events of axonal regeneration in a different context.…”

Bilateral Consequences of Chronic Unilateral Deafferentation in the Auditory System of the Cricket <i>Gryllus bimaculatus</i>

“…Observations in a variety of species have led to the hypothesis that each neuron is predetermined to be a particular size [Schneider, 1973;Devor, 1975]. For example, axotomy or changes in afferent innervation induce changes in dendritic arbors that appear to be balanced by reciprocal changes in other regions [Shankland et al, 1982;Roederer and Cohen, 1983;Hall and Cohen, 1988]. Our results indicated an overall decrease in dendritic complexity, and one could speculate that the total volume was thus reduced after deafferentation as well.…”