Serial electron microscopic reconstruction of axon terminals on physiologically identified thalamocortical neurons in the cat ventral lateral nucleus.

Abstract

The distribution of different types of terminals on different portions of single thalamocortical neurons (TCNs) was quantitatively investigated in the cat ventral lateral nucleus (VL) by the application of computer-assisted three-dimensional reconstruction from serial ultrathin sections. Single neurons in the VL were intracellularly penetrated with a glass micropipette filled with horseradish peroxidase (HRP), and were electrophysiologically identified as TCNs by their antidromic responses to stimulation of the motor cortex. These TCNs received monosynaptic excitation from the contralateral cerebellum. After electrophysiological identification, they were injected with HRP iontophoretically. The spatial distribution of terminals of different types on two identified TCNs was analyzed on serial ultrathin sections, some of which were stained by a postembedding immunogold technique by using a gamma-aminobutyric acid (GABA) antibody. Terminals that synapsed on the injected cells were categorized as LR terminals (GABA-negative large axon terminals containing round vesicles), SR terminals (GABA-negative small axon terminals containing round vesicles), P terminals (GABA-positive axon terminals of various sizes containing pleomorphic vesicles), or PSDs (presynaptic dendrites). The order of dendritic branches of labeled TCNs was determined by computer-assisted reconstruction from serial sections. LR terminals made contacts mainly with proximal dendrites of TCNs. SR terminals made contacts predominantly with distal dendrites, and were never found on somata or primary dendrites. P terminals were observed on somata and on every portion of the dendritic trees. Synapses formed by PSDs were concentrated on the proximal dendrites and sometimes formed synaptic triads with LR terminals. Only a few terminals were found on somata, all of which were P type. Therefore, terminals belonging to different classes were not uniformly distributed on the somata and dendrites of single TCNs. These results suggest that terminals originating from different sources may preferentially contact specific regions of TCNs in the VL, and their topographical locations reflect the electrophysiological response properties of the TCNs.