Synaptology of trigemino‐ and spinothalamic lamina I terminations in the posterior ventral medial nucleus of the macaque

Abstract

We used the electron microscope to examine lamina I trigemino- and spinothalamic (TSTT) terminations in the posterior part of the ventral medial nucleus (VMpo) of the macaque thalamus. Lamina I terminations were identified by anterograde labeling with biotinylated dextran, and 109 boutons on 38 terminal fibers were closely studied in series of ultrathin sections. Five unlabeled terminal boutons of similar appearance were also examined in detail. Three-dimensional, volume-rendered computer models were reconstructed from complete series of serial sections for 29 boutons on 10 labeled terminal fibers and one unlabeled terminal fiber. In addition, postembedding immunogold staining for GABA was obtained in alternate sections through 23 boutons. Lamina I TSTT terminations in VMpo generally have several large boutons (mean length = 2.16 microm, mean width = 1.29 microm) that are densely packed with vesicles and make asymmetric synaptic contacts on low-order dendrites of VMpo neurons (mean diameter 1.45 microm). They are closely associated with GABAergic presynaptic dendrites (PSDs), and nearly all form classic triadic arrangements (28 of 29 reconstructed boutons). Consecutive boutons on individual terminal fibers make multiple contacts with a single postsynaptic dendrite and can show evidence of progressive complexity. Dendritic appendages that enwrap and invaginate the terminal bouton constitute additional anatomic evidence for secure, high-fidelity synaptic transfer. These observations provide direct ultrastructural evidence supporting the hypothesis that VMpo is a lamina I TSTT thalamocortical relay nucleus in primates that subserves pain, temperature, itch, and other sensations related to the physiological condition of the body.

Retrograde analyses of spinothalamic projections in the macaque monkey: Input to posterolateral thalamus

“…Briefly, preceding anatomical evidence indicates that VMpo is a cytoarchitectonically and immunohistochemically distinguishable region in the posterolateral thalamus of monkeys and humans (Craig et al, 1994;Blomqvist et al, 2000;Craig, 2004) that receives dense clusters of lamina I terminal arbors that bear large, glutamatergic boutons organized in triadic arrangements with proximal postsynaptic dendrites and GABAergic presynaptic dendrites (Beggs et al, 2003). Physiological evidence in monkeys indicates that VMpo neurons are organized in clusters that show nociceptive-specific and thermoreceptive-specific responses similar to those of lamina I neurons (Craig et al, 1994(Craig et al, , 1999(Craig et al, , 2001.…”

Role of primary somatosensory cortex in the coding of pain

“…A projection which does not fit this pattern , from HPC lamina I cells to thalamic nucleus VMpo [28], has been challenged on technical grounds [55;141]. Even though subsequent anatomical studies established the validity of a lamina I projection to VMpo [8;32;97], the classical view persists – i.e., that SI processing of pain occurs in areas 3b and 1. Craig and Blomqvist (2002), for example, viewed the projection from VMpo to area 3a as a “corollary track” subserving sensorimotor integration.…”

Topographically organized projection to posterior insular cortex from the posterior portion of the ventral medial nucleus in the long‐tailed macaque monkey

“…It was named the posterior part of the ventral medial nucleus (VMpo), because together with the contiguous basal part of the ventral medial nucleus (VMb), it constitutes a topographically coherent structure that receives ascending input representative of all interoceptive (homeostatic sensory) activity (Beckstead et al, 1980; Pritchard et al, 2000). The lamina I terminations in VMpo consist of dense clusters of large boutons that are glutamatergic (Blomqvist et al, 1996) and form triadic synaptic complexes characteristic of thalamic relay nuclei (Beggs et al, 2003). Thus, microelectrode recordings that revealed clusters of thermoreceptive-specific (COOL) and nociceptive-specific (NS) neurons in VMpo that are topographically organized with the same antero-posterior gradient (head to foot) naturally suggested that VMpo could serve as a specific relay nucleus for pain and temperature sensations (Craig et al, 1994).…”