Ultrastructural changes in cockroach leg muscle following unilateral neurotomy. I. Degeneration

Abstract

Neurotomized retractor unguis (R.u.) muscles of adult male cockroaches, Periplaneta americana , were examined electrophysiologically and ultrastructurally. Miniature excitatory postsynaptic potentials (min EPSPs) were recorded intracellularly for up to 96 hr after neuromuscular transmission had failed. The miniature discharge declined gradually during this period and by 4–6 days postneurotomy at 25°C the majority of muscles were electrically silent. Neither “bursts” nor “giant” miniature potentials were recorded from neurotomized muscles. The cessation of miniature discharge was correlated with glial cell engulfment of axon terminals. The occurrence of dense aggregates of synaptic vesicles in degenerating terminals was invariably accompanied by the isolation of such terminals from the aposynaptic apparati by glial cells. Following complete terminal degeneration, glial cells remained in close proximity to persistent aposynaptic apparati. However, there was no resumption of miniature activity without clear evidence of reinnervation having occurred. The neurotomized R.u. muscles showed a marked increase in glycogen granules during the first week and muscle dry weight measurements indicated a 15% hypertrophy during this period. During the second week following neurotomy, extensions from the R.u. muscle fiber developed at former junctional sites. These extensions possessed isolated cisternae of SR, dyads, microtubules, ribosomes, and glycogen granules. From about 12 days postneurotomy, specialized associations were observed between contiguous myofibers. These associations, considered to be adherens junctions, became more pronounced as muscle atrophy progressed and persisted until such time as the myofibers were reinnervated. By 20 days postneurotomy, a reduction in sarcoplasmic reticulum was apparent with a concomitant loss of myofibrillar substructure. At 30 days, mitochondrial breakdown and a loss of superficial myofilaments was evident and by 40 days postneurotomy, muscle dry weight had decreased by 35–40%. Muscle atrophy continued steadily thereafter providing that reinnervation did not occur.