Pathfinding, target recognition, and synapse formation of single regenerating fibers in the adult grasshopper Schistocerca gregaria

After lesion of the peripheral tympanal nerve of the adult locust (Schistoc erca gregaria), sensory axons regenerate into their original target areas. We examined the individual behavior of single regenerating auditory afferen ts during pathway and target selection by intracellularly recording and lab eling them at different times postlesion. During axotomy, spontaneous activ ity is not increased in either the distal or proximal part of the cells. St imulus response properties of lesioned cells with or without regenerating a xons are not influenced, Surprisingly, only 55% of sensory neurons regenera te through the lesion site and often give rise to more than one axonal fibe r. Within the central nervous system, 70% of regenerated axons consistently follow an incorrect pathway to reach the correct target region. Often, one of two processes formed by a cell chooses the correct pathway, and the oth er the incorrect one, In the target region, regenerated axons reconstitute somatotopically ordered projections and form synapses that resemble those o f intact fibers in number and structure, The regeneration process does not induce a detectable expression of antigens that are known to be expressed d uring neural dt development in these neurons. Our study clearly demonstrate s that precise synaptic regeneration is possible in adult animals within a completely differentiated central nervous system, although pathfinding and formation of arborizations are disturbed in a particular and probably syste m-related manner, The results strongly suggest that accurate pathfinding is unlikely to be a decisive factor in target area recognition and synaptogen esis. (C) 2000 John Wiley & Sons, Inc.