Recent commentaries on the role of the thalamus consider a wide sphere of influence beyond sensory-motor transformation, to include task-relevant cognitive processes. In this short review, I reconsider known anatomic features of corticothalamic connectivity, primarily for macaque monkey, and discuss these as part of an intricate network architecture consistent with multiple connectional recombinations and a diversity of functional tasks. Drawing mainly on results from single axon analysis for the two broad classes of corticothalamic (CT) connections, I review the strikingly complementary spatial parameters of their extrinsic CT arbors in relation to intrinsic cortical collaterals. That is, CT neurons in layer 5 (class II) have spatially compact (low divergent) thalamic fields, but highly spatially divergent cortical collaterals. In contrast, CT neurons in layer 6 (class I) have highly divergent thalamic fields, but delimited, low divergent cortical collaterals. CT convergence in the thalamus is technically more difficult to analyze, but one can infer a low convergence of terminations from layer 5, in contrast with CT terminations from layer 6, which are highly convergent. Reciprocating thalamocortical (TC) axons have multiple clustered and divergent arbors. What to conclude from these relationships requires further investigation of activity patterns and networks under different conditions. Specific parameters are suggestive of selective recruitment of distributed postsynaptic networks and ordered activity sequences; but are these separable systems, operating cooperatively or in parallel (L.5 low divergent/low convergent vs. L. 6 high divergent/high convergent)?