Morphology and connections of intratrigeminal cells and axons in the macaque monkey

The terminal areas and cells of origin of the somatosensory projection to the mesencephalon in the monkey were investigated by the intraaxonal transport method. Following injection of wheat germ agglutinin-horseradish peroxidase conjugate (WGA-HRP) into the spinal enlargements, the lateral cervical nucleus (LCN), the dorsal column nuclei (DCN), or the spinal trigeminal nucleus, anterograde labeling was observed in several regions of the mid-brain. (1) Injection of tracer into the spinal enlargements resulted in dense terminal labeling in the parabrachial nucleus (PBN) and the periaqueductal gray matter (PAG); moderate termination was observed in the intercollicular nucleus (Inc), the intermediate and deep gray layers of the superior colliculus (SGI, SGP), the posterior pretectal nucleus (PTP), and the nucleus of Darkschewitsch (D); and scattered terminal fibers were seen in the cuneiform nucleus (CNF) and the pars compacta of the anterior pretectal nucleus (PTAc). The projections from the cervical enlargement to PAG, Inc, and the superior colliculus terminated more rostrally than those from the lumbar segments, indicating a somatotopic organization. (2) Terminal labeling after injection of tracer into LCN was found mainly in Inc, SGI, and SGP, but sparse labeling was also observed in the nucleus of the brachium of the inferior colliculus (BIN), PAG, PBN, PTP, and D. (3) The projection from DCN terminated densely in the external and pericentral nuclei of the inferior colliculus (ICX, ICP), Inc, SGI, SGP, PTP, PTAc, the nucleus ruber, and D, and weak terminal labeling was seen in BIN, PAG, and PBN. Comparisons of the anterograde labeling following injections involving both the gracile nucleus and the cuneate nucleus with that after injection restricted to the gracile nucleus alone suggested a somatotopic termination pattern in Inc, the superior colliculus, and the pretectal nuclei. (4) The patterns of projection from the laminar and alaminar parts of the spinal trigeminal nucleus differed: injection of tracer into the caudal part of the alaminar spinal trigeminal nucleus (nucleus interpolaris) resulted in dense anterograde labeling in SGI and SGP, moderate termination in Inc, and minor projections to PBN, PAG, and PTP, whereas after tracer injection into the laminar trigeminal nucleus (nucleus caudalis) terminal labeling was present only in PBN and PAG. Following injection of tracer into the midbrain terminal areas retrogradely labeled neurons were found in the spinal cord, LCN, DCN, and the spinal trigeminal nucleus, with the majority of labeled cells situated on the side contralateral to the injection site.(ABSTRACT TRUNCATED AT 400 WORDS)

Trigeminal sensory nuclei are the first processing stage in the vibrissal system of rodents. They feature separate populations of thalamic projecting cells and a rich network of intersubnuclear connections, so that what is conveyed to the cortex by each of the ascending pathways of vibrissal information depends on local transactions that occur in the brainstem. In the present study, we examined the nature of these intersubnuclear connections by combining electrolytic lesions with electrophysiological recordings, retrograde labeling with in situ hybridization, and anterograde labeling with immunoelectron microscopy. Together, these different approaches provide conclusive evidence that the principal trigeminal nucleus receives inhibitory GABAergic projections from the caudal sector of the interpolaris subnucleus, and excitatory glutamatergic projections from the caudalis subnucleus. These results raise the possibility that, by controlling the activity of intersubnuclear projecting cells, brain regions that project to the spinal trigeminal nuclei may take an active part in selecting the type of vibrissal information that is conveyed through the lemniscal pathway.

1. A total of 113 trigeminothalamic neurons and over 200 presumed interneurons of nucleus caudalis (0-5 mm below the obex) and subjacent reticular formation were studied in rhesus monkeys anesthetized with chloralose or nitrous oxide. Each cell was characterized in terms of its antidromic responses to stimulation of ventral posterior medial and/or posterior thalamic nuclei and to three types of stimuli applied to its receptive field: a) graded 5-s temperature shifts at a rate of 9 degrees C/s from 35 degrees C to final temperatures of 20-52 degrees C, generated by a contact thermode; b) graded intensities of electrical stimulation to determine the conduction velocities of converging primary afferent fiber populations; and c) mechanical stimulation ranging from light touch to pinch with serrated forceps. 2. This analysis yielded five classes of units distinguished by the range of responses to mechanical stimuli and by the convergence of different primary afferent fiber populations. These five classes were found among both trigeminothalamic neurons and neurons which could not be antidromically activated. Class 1 units exhibited rapidly adapting responses to hair movement or light touch and received only A-beta primary afferent input. Class 2 units responded to light touch and pressure with maintained discharges and received A-beta primary afferent input. Class 3 units responded maximally to pinch with serrated forceps but also were activated by light touch and pressure. They received A-beta, A-delta, and C fiber input. Class 4 units responded to firm pressure and maximally to pinch with serrated forceps. These units had A-delta and sometimes C fiber input. Class 5 units responded only to pinch with serrated forceps and had exclusive A-delta fiber input. Some cells in all five classes responded antidromically to stimulation of the thalamus. Antidromic action-potential latencies of classes 1,2, and 3 units were shorter than those of classes 4 and 5 units (P less than 0.001). Receptive-field sizes were usually small (1-2 cm2) for classes 1, 2, 4, and 5 units, and larger for class 3 units (one to three trigeminal divisions). The marginal layer of nucleus caudalis contained mostly classes 4 and 5 units, some class 3 units, but no classes 1 or 2 units. The superficial portion of the magnocellular layer contained mostly classes 1 and 2 units, while neurons at the base of this layer contained class 3 units and some classes 4 and 5 units. Cells in the sujacent reticular formation included all 5 classes but showed a tendency to have large receptive fields (greater than 1 trigeminal division). 3. Neurons responding to noxious thermal stimuli (44-52 degrees C) were classes 3 or 4 units. The response patterns of classes 3 and 4 units to noxious thermal stimuli were similar. No classes 1 or 2 units and only one class 5 unit responded to increases in skin temperature. Thermal thresholds ranged from 38 to 50 degrees C and most heat-responsive units responded monotonically to temperatures between 45 and 52 degrees C...