Synaptic organization of nociceptive relay nuclei in the cat and primate thalamus

• The fine structure of two thalamic nociceptive relay nuclei, the nucleus submedius (Sm) in the cat, and the posterior region in the owl monkey, was investigated using anatomical tract tracing techniques, immunohistochemical staining for neuroactive substances, and threedimensional reconstructions of synaptic circuitry. Ascending lamina I axons, labeled by anterograde transport of Phaseolus vulgaris leucoagglutinin, gave rise to two different types of termination in Sm: large, compact clusters of numerous boutons were predominant in the dense focus of the terminal field after a tracer injection at the site of nociceptive-specific neurons in lamina I, and boutons-of-passage type terminations were conspicuous in the periphery of a lamina I terminal field in Sm and predominant following a tracer injection at the site of thermoreceptive-specific neurons in lamina I. Three-dimensional reconstructions of a sample of these terminations, generated from series of ultrathin sections by using special software on a computer workstation, showed that all boutons of each cluster made synaptic contact with protrusions and branch points on a single dendrite. These contacts involved presynaptic dendrites (PSDs) in triadic arrangements. In contrast, the boutons-of-passage type terminations were generally characterized by contacts with PSDs, and some of the passing varicosities made simple such synaptic contacts. However, an intermediate termination pattern was also found in which boutons-of-passage fanned synaptic complexes with dendritic appendages involving PSD contacts. Postembedding immunogold-labeling techniques showed that the spinal and trigeminal terminals in Sm contained synaptic vesicle-associated glutamate, suggesting that glutamate is an excitatory neurotransmitter in these terminals. Corticothalamic tract terminals were also glutamatergic. Immunoreactivity to gamma-aminobutyric acid (GABA) was observed in PSDs originating from GABAergic intrinsic neurons and in axon tenninals supposed to originate from the reticular thalamic nucleus. A similar organization of glutamatergic and GABAergic elements was seen in the posterior thalamic region of owl monkeys. The different types of synaptic organization seen in Sm are consistent with the possibility that modality-selective nociceptive and thermoreceptive lamina I neurons terminate differentially in this nucleus and suggest a functional integration of cold and pain activity. The presentfindings provide evidence that such activity is transmitted by the excitatory amino acid glutamate and is modulated by inhibitory GABAergic mechanisms. Glutamate and GABA are also involved in the processing of ascending information in the posterior thalamic region of owl monkeys, showing that these substances are important for pain transmission in primates as well.

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