Single- and Multi-Whisker Channels in the Ascending Projections from the Principal Trigeminal Nucleus in the Rat

Abstract

This study investigated the relationship between axonal projections and receptive field properties of whisker-sensitive cells in the principal trigeminal sensory nucleus of the rat. The labeling of small groups of trigeminothalamic axons with biotinylated dextran amine disclosed two broad classes of axons; a majority of fibers (68%; n ϭ 107) project to a single barreloid of the ventral posteromedial nucleus, and the remaining group includes axons that innervate both the posterior group of the thalamus and the tectum. Additional terminal sites for axons of this latter group may include the pretectum, the zona incerta, the medial part of the medial geniculate nucleus, and the ventral posteromedial nucleus. Corresponding to these two classes of fibers, 67% of the cells in the principal trigeminal nucleus (n ϭ 313) have single-whisker receptive fields, whereas the rest of the population have receptive fields composed of multiple whiskers. The tonic or phasic properties of the responses apparently bear no relation to the axonal projection patterns. Solid retrograde labeling of cells that project to the ventral posteromedial nucleus and intracellular staining revealed that single-whisker cells have small somata and narrow, barrelette-bounded dendritic trees. In contrast, multi-whisker neurons have large multipolar somata, expansive dendritic trees, and many respond antidromically to stimulation of the superior colliculus. Together, these results provide evidence for two main channels of vibrissal information: a single-whisker channel that links trigeminal barrelettes to their corresponding barreloids, and a multi-whisker channel that distributes principally in the posterior group and tectum. Key words: vibrissa; barrel system; trigeminothalamic afferents; superior colliculus; posterior group nuclei; principal trigeminal nucleusThe rodent somatic sensory system is characterized by a prominent representation of the mystacial vibrissae. On each side of the rat snout, there are five horizontal rows of whiskers that form an orderly array of low-threshold mechanoreceptors. Each peripheral fiber innervating these mechanoreceptors responds to only one vibrissa and, centrally, the arrangement of the vibrissal pad is maintained in arrays of cellular aggregates referred to as barrelettes (brainstem), barreloids (thalamus), and barrels (cortex).Brainstem nuclei that receive vibrissal primary afferents include the principal trigeminal nucleus (Pr5) and all subdivisions of the spinal trigeminal complex. Each of these (sub)nuclei contributes axons to the trigeminothalamic tract, but the main stream of ascending afferents arise from the Pr5 and interpolar division of the spinal complex. Many studies have investigated the responses of first-order afferents, thalamic, and cortical cells to vibrissae deflection (Armstrong-James, 1995;Diamond, 1995;Simons, 1995). In contrast, few physiological works have been devoted to the trigeminothalamic cells of the Pr5. The most comprehensive study (Shipley, 1974) described two broad classes of neu...

Essential role of postsynaptic NMDA receptors in developmental refinement of excitatory synapses

“…4 A and C). The pattern of VGluT2 innervation at P14 was comparable with those reported for Pr5 axonal terminals in the VPm of adult rats (35,36). These results suggest that the refinement of vibrissal relay synapses in the VPm is associated with pruning of somatic innervation by Pr5 axons.…”

A New Thalamic Pathway of Vibrissal Information Modulated by the Motor Cortex

“…This conclusion is consistent with our previous single-axon tracing study in which we reported that the dorsal part of the VPM receives input from two types of PrV cells: cells with a mono-whisker receptive field that form small clusters of terminals in a single barreloid and large multiwhisker-responsive cells that innervate Po and the dorsalmost sector of multiple barreloids (Veinante and Deschênes, 1999) A previous study already demonstrated that cells in the tail of the barreloids project to S2 and to the dysgranular zone of S1 (Pierret et al, 2000). If cells in the head and core of the barreloids form separate pathways of vibrissal information, one would expect both populations of neurons to also differ in the way they innervate barrel cortex.…”

“…In addition, several anatomical studies have pointed out to a functional specialization of the dorsalmost part of the barreloids that abuts Po (hereinafter referred to as the head of the barreloids). This region receives input from specific sets of PrV, reticular thalamic, and corticothalamic fibers (Bourassa et al, 1995;Deschênes et al, 1998;Veinante and Deschênes, 1999;Désîlets-Roy et al, 2002), and it was also proposed that cells in the head of the barreloids might receive corticothalamic input from the motor cortex (Deschênes et al, 1998). Yet, no physiological study has reported distinct response properties for cells located in the head of the barreloids.…”

Properties of the thalamic projection from the posterior medial nucleus to primary and secondary somatosensory cortices in the mouse

“…It has been well documented in in vivo studies that stimulation of whiskers activates both the lemniscal and paralemniscal pathways resulting in responses throughout S1 in both barrels and septa (1,2,14,15). In the paralemniscal pathway, POm receives ascending sensory input from the subnuclei of the spinal trigeminal complex (27,28). POm receives Class 1A input from layer 5 of S1 (29) and also receives input from layers 5 and 6 of S2 (30).…”