Deafferentation effects in lateral cuneate nucleus of the cat: Correlation of structural alterations with firing pattern changes

Abstract

A correlated anatomical and physiological investigation of the effects of unilateral cervicothoracic dorsal rhizotomies upon lateral cuneate nucleus of the cat (LCN) is reported. Pairs of adult cats with identical survival times were selected to correlate structural and functional changes. Two phases are described in the development of alterations of neuronal firing patterns. In the first phase, a relative silence within LCN was associated with depletion of round synaptic vesicles in the presynaptic profiles (LR boutons) of primary dorsal root afferents. The second phase was characterized by a development of spontaneous electrical hyperactivity which corresponded anatomically to the presence of denuded postsynaptic specializations, transient increase of adjacent extracellular space and an apparent decrease in the number of dendritic spines. There was a persistence of an unaltered population of small presynaptic boutons with flattened vesicles (SF boutons). The LCN neuronal membrane is viewed as having an intrinsic tendency for repetitive firing which is enhanced by the functional effects of denuded postsynaptic specialization. A marked similarity was found between some of the spontaneous firing patterns of normal animals (doublets) and the high frequency bursting firing pattern in deafferented preparation. Three models for repetitive spike production are considered in our analysis: oscillator-produced spikes; EPSP-produced spikes; and spike-evoked spikes. The spike-evoked spikes model is considered to be the origin of normal doublet activity and a candidate for the deafferented burst activity. Abnormal hyperactivity after deafferentation may be a function of changes in the membrane characteristics occurring at or near the denuded postsynaptic specializations.