Medial lemniscal and spinal projections to the macaque thalamus: an electron microscopic study of differing GABAergic circuitry serving thalamic somatosensory mechanisms.
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.
Ralston
H J
HJ
Department of Anatomy, W. M. Keck Foundation Center for Integrative Neuroscience, University of California, San Francisco 94143-0452.
Ralston
D D
DD
D000344:Afferent Pathways / Q000033:anatomy & histology / Q000648:ultrastructure; D000818:Animals; D001370:Axonal Transport; D003196:Computer Graphics; D003712:Dendrites / Q000648:ultrastructure; D006735:Horseradish Peroxidase; D008252:Macaca fascicularis / Q000033:anatomy & histology*; D008297:Male; D008854:Microscopy, Electron / Q000379:methods; D008953:Models, Anatomic; D009411:Nerve Endings / Q000648:ultrastructure; D009474:Neurons / Q000648:ultrastructure*; D013569:Synapses / Q000648:ultrastructure*; D013787:Thalamic Nuclei / Q000033:anatomy & histology / Q000648:ultrastructure*; D013788:Thalamus / Q000033:anatomy & histology / Q000648:ultrastructure*; D018998:Wheat Germ Agglutinin-Horseradish Peroxidase Conjugate; D014909:Wheat Germ Agglutinins; D005680:gamma-Aminobutyric Acid / Q000032:analysis*
D018998:Wheat Germ Agglutinin-Horseradish Peroxidase Conjugate; D014909:Wheat Germ Agglutinins; D005680:gamma-Aminobutyric Acid; D006735:Horseradish Peroxidase