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Axon Regeneration In The Lamprey Spinal Cord

M. Shifman, M. Selzer
Published 2015 · Biology

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The lamprey has been used to distinguish regeneration from collateral sprouting in a true vertebrate central nervous system (CNS). (1) Animals recover and can be studied after complete spinal transection (TX), so that regeneration past the lesion is unambiguous. (2) Identified neurons in brain and spinal cord can be visualized in vivo and in CNS whole mounts. Fluorescently labeled axons can be followed and the structure of their distal tips discerned during regeneration in living animals. (3) The spinal projecting neurons of the lamprey brain have been characterized with regard to their anatomical projections, their synaptic connections to neurons in the spinal cord, their roles in locomotion and their regenerative abilities. (4) Molecular expression patterns can be correlated with regenerative abilities in individually identified giant reticulospinal neurons and in clusters of smaller spinal projecting neurons. (5) Drugs and even large molecules can penetrate to the center of the cord after surface application. (6) Perhaps most importantly, axon regeneration is robust but not complete. About half of the spinal projecting axons regenerate beyond the lesion by 12 weeks post-TX and these regenerate only a few millimeters rather than all the way back to their previous caudalmost targets. Thus there is equal room for molecular and pharmacological manipulations to enhance or inhibit regeneration, i.e., experiments are not hindered by floor or ceiling effects. These advantages have been used to discover several important features of regeneration that may well apply to mammalian species as well. (a) Regeneration of the axons of large, identified neurons of the brain and spinal cord is specific with regard to pathfinding and synaptic reconnection, so that it can be assumed that sufficient specificity cues persist in the developed nervous system to underlie recovery if a sufficient amount of regeneration could be achieved. (b) The mechanism of axon elongation during regeneration does not involve the actin–myosin molecular motor that underlies growth cone pulling in early embryonic axon outgrowth. Instead the growing axon tips are simple in shape, lack filopodia, have relatively little F-actin, and are tightly packed with neurofilaments. This is important because much of the work on therapeutic approaches to promote regeneration has been predicated on the assumption that regeneration recapitulates the mechanisms of embryonic axonal development. (c) The heterogeneity in the abilities of neurons to regenerate their axons through the same environment means that axon regeneration is determined not only by environmental factors, but also by neuron-intrinsic differences. Some of these include differences in the expression of cytoskeleton, transmembrane receptors, and sensitivity to axotomy-induced retrograde apoptosis.
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