Dendroarchitecture of relay cells in thalamic barreloids: a substrate for cross-whisker modulation

A double-labeling protocol was used to determine how the dendroarchitecture of relay cells relates to the three-dimensional structure of barreloids in the ventral posterior medial nucleus of the rat thalamus. Single barreloids were retrogradely labeled by injecting Fluoro-Gold in identified barrel columns, and single relay cells activated by the same whisker, or by an adjacent whisker located on the same arc, were juxtacellularly labeled with biotinylated dextran. Results show that the dendritic field of relay cells is asymmetric, variously oriented with respect to the geometry of the barreloids, and that all cells extend dendrites in surrounding barreloids. Extrabarreloid dendrites are of small size (<1.5 microm) and represent up to 54% (range, 11-54%) of the total dendritic length. In contrast, the thick proximal dendrites remain confined to the home barreloid of the cell, being directed toward its center or along its margin. There is a trend for cells located dorsally in barreloids to form more elaborate trees with a larger proportion of extrabarreloid dendrites. Electron microscopic examination of labeled cells shows that extrabarreloid dendrites are exclusively contacted by synaptic terminals of cortical and reticular thalamic origin, whereas intrabarreloid dendrites also receive contacts from lemniscal terminals. Because corticothalamic and reticular thalamic cells establish point-to-point connections with homotopic barreloids, it is proposed that the spatial arrangement of dendrites determines the combination of whisker deflection that best modulates cell firing. Because relay cell responses are direction sensitive, maximal modulation would occur if dendritic field orientation relates to the direction selectivity of responses.