Differential Foci and Synaptic Organization of the Principal and Spinal Trigeminal Projections to the Thalamus in the Rat

The thalamus is known to receive single-whisker ‘lemniscal’ inputs from the trigeminal nucleus principalis (Prv) and multiwhisker ‘paralemniscal’ inputs from the spinal trigeminal nucleus (Spv), yet the responses of cells in the thalamic ventroposteromedial nucleus (VPM) are most similar to and contingent upon inputs from PrV. This may reflect a differential termination pattern, density and/or synaptic organization of PrV and SpV projections. This hypothesis was tested in adult rats using anterograde double-labelling with fluorescent dextrans, horseradish peroxidase (HRP) and choleragenoid, referenced against parvalbumin and calbindin immunoreactivity. The results indicated that Prv's most robust thalamic projection is to the whisker-related barreloids of VPM. The SpV had robust projections to non-barreloid thalamic regions, including the VPM ‘shell’ encapsulating the barreloid area, a caudal and ventral region of VPM that lacks barreloids and PrV inputs, the posterior thalamic nucleus, nucleus submedius and zona incerta. Within the barreloid portion of VPM, SpV projections were sparse relative to those from PrV, and most terminal labelling occurred in the peripheral fringes of whisker-related patches and in inter-barreloid septae. Thus, PrV and SpV have largely complementary projection foci in the thalamus. Intra-axonal staining of a small sample of trigeminothalamic axons with whisker or guard hair receptive fields revealed highly localized and somatotopic terminal aggregates in VPM that spanned areas no larger than that of a single barreloid. In the electron microscopic component of this study, HRP transport to the barreloid region of VPM from left SpV and right PrV in the same cases revealed PrV terminals contacting dendrites with a broad range of minor axis diameters (mean ± SD: 1. 51 ± 0. 10 μm). SpV terminals were indistinguishable from those of PrV, but they had a disproportionate number of contacts on narrow dendrites (1. 27 ± 0. 07 μm, P 0. 01). PrV endings were also more likely to contact VPM somata (11. 0 ± 4. 2% of all labelled terminals) than those from SpV (3. 0 ± 1. O%, P 0. 01). Insofar as primary dendrites are thicker than distal dendrites in VPM, these data suggest a differential distribution of PrV and SpV inputs onto VPM cells that may account for their relative efficacies in dictating the responses of VPM cells to whisker stimulation. Multiwhisker receptive fields in VPM may also reflect direct transmission of convergent inputs from PrV.