Journal of Neuroscience, Vol 14, 2485-2502, Copyright © 1994 by Society for Neuroscience
Medial lemniscal and spinal projections to the macaque thalamus: an electron microscopic study of differing GABAergic circuitry serving thalamic somatosensory mechanisms
HJ Ralston 3rd and DD Ralston
Department of Anatomy, W. M. Keck Foundation Center for Integrative Neuroscience, University of California, San Francisco 94143-0452.
The synaptic relationships formed by medial lemniscal (ML) or spinothalamic
tract (STT) axon terminals with neurons of the somatosensory
ventroposterolateral thalamic nucleus of the macaque monkey have been
examined quantitatively by electron microscopy. ML and STT axons were
labeled by the anterograde axon transport of WGA-HRP following injection of
the tracer into the contralateral dorsal column nuclei, or the dorsal horn
of the spinal cord, respectively. Thalamic tissue was histochemically
reacted for the presence of HRP. Serial thin sections were stained with a
gold-labeled antibody to GABA, to determine which neuronal elements
exhibited GABA immunoreactivity (GABA- ir). Serially sectioned thalamic
structures were recorded in electron micrographs and reconstructed in three
dimensions by computer. Individual ML axon terminals form multiple synaptic
contacts with segments of the proximal dendritic trees of thalamocortical
relay neurons and also synapse upon the dendritic appendages of GABA-ir
interneurons (local circuit neurons). These GABA-ir dendritic appendages
contain synaptic vesicles and are presynaptic (presynaptic dendrites) to
the same segments of relay neuron dendrites that receive ML contacts. When
analyzed in serial sections and reconstructed by computer, the ML terminals
form triadic relationships (ML, GABA appendage, and relay neuron dendrite)
or more complex glomerular arrangements involving multiple appendages, all
of which then contact the relay neuron dendritic segment. In contrast,
multiple STT terminals make synaptic contacts along segments of projection
neuron dendrites and are usually the only type of profile to contact that
segment of dendrite. More than 85% of the spinal afferents form simple
axodendritic synapses with relay cells and do not contact GABA-ir
appendages. The thalamic synaptic relationships of ML terminals are
fundamentally different from those formed by the STT. Because STT neurons
predominatly transmit information about noxious stimuli, the simple
axodendritic circuitry of the majority of these spinal afferents suggests
that the transmission of noxious information is probably not subject to
GABAergic modulation by thalamic interneurons, in contrast to the GABAergic
processing of non-noxious information carried by the ML afferents. The
differences in the GABAergic circuits of the thalamus that mediate ML and
STT afferent information are believed to underlie differential
somatosensory processing in the forebrain. We suggest that changes in
thalamic GABAergic dendritic appendages and GABA receptors following CNS
injury may play a role in the genesis of some central pain states.
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