Morphology of superior colliculus- and middle temporal area-projecting neurons in primate primary visual cortex

Layers 5 and 6 of primate primary visual cortex (V1) harbor morphologically diverse cell groups that have corticocortical and corticosubcortical projections. Layer 6 middle temporal area (MT)-projecting neurons are particularly interesting, as they are the only deep-layer cortical neurons that provide both corticocortical feedforward inputs (to area MT) and corticosubcortical feedback projections (to superior colliculus [SC]) (Fries et al. [1985] Exp Brain Res 58:613-616). However, due to limitations in anatomical tracing techniques, little is known about the detailed morphologies of these cells. We therefore applied a genetically modified rabies virus as a retrograde tracer to fill the dendrites of projection neurons with green fluorescent protein (GFP) (Wickersham et al. [2007] Nat Methods 4:47-49). We injected virus into SC or area MT of macaque monkeys and examined labeled cells in V1. Two-thirds of labeled neurons following SC injections were found in layer 5, consisting of "tall-tufted" and "nontufted" cells; the remaining cells were layer 6 "nontufted." Area MT injections labeled neurons in layers 4B and 6, as previously described (Shipp and Zeki [1989] Eur J Neurosci 1:309-332). The layer 6 neurons projecting to MT were remarkably similar to the layer 6 SC-projecting neurons. In contrast to the dense and focused dendritic arbors of layer 5 "tall-tufted" pyramids, all "nontufted" cells had sparse, but unusually long basal dendrites. The nontufted cells closely resemble Meynert cells (le Gros Clark [1942] J Anat 76:369-376; Winfield et al. [1983] Proc R Soc Lond B Biol Sci 217:129-139), but the full in vivo reconstructions presented here show that their basal dendrites can extend much further (up to 1.2 mm) and are less asymmetric than inferred from Golgi reconstructions.