Functional streams and local connections of layer 4C neurons in primary visual cortex of the macaque monkey

Abstract

The primate visual system is composed of multiple, functionally specialized cortical areas. The functional diversity among areas is thought to reflect different contributions from early parallel visual pathways to the area V1 neurons providing input to 'higher' cortical areas. The M pathway is believed to provide information about motion and contrast, via layer 4B of V1, to dorsal visual areas. The P pathway is believed to provide information about shape and color, via layer 2/3 of V1, to ventral visual areas, with specialized contributions from cytochromeoxidase (CO) blob versus interblob neurons. However, the detailed anatomical relationships between the M and P pathways and the neurons in V1 that provide input to higher extrastriate cortical areas are poorly understood. To study these relationships, spiny stellate neurons in the M- and P-recipient layers of V1, 4Cα and 4Cβ, respectively, were intracellularly labeled, and their axonal and dendritic arbors were reconstructed. We find that neurons with dendrites in upper layer 4Cα project axons to layer 4B and CO blobs in layer 2/3, thus relaying M input to these regions. Other neurons in lower layer 4Cα provide M input to interblobs. These cells have either (1) dendrites restricted to lower layer 4Cα and axons specifically targeting layer 2/3 interblobs, or (2) dendrites in lower 4Cα and 4Cβ and axons targeting blobs and interblobs. P-recipient layer 4Cβ neurons have dense axonal arbors in both blobs and interblobs but not layer 4B. Quantitative analyses reveal that 4Cα cells provide approximately five times more synapses than 4Cβ cells to layer 4B, whereas 4Cβ cells provide five times more synapses than 4Cα cells to layer 2/3. These observations imply that M input is dominant in layer 4B. In layer 2/3, both blobs and interblobs receive M and P input, but the P input is dominant, and M input to interblobs derives exclusively from a subpopulation of M afferents that targets lower 4Cα, not from afferents targeting only upper 4Cα (cf. Blasdel and Lund, 1983). We speculate that the M and P pathways to interblobs are 'X-like' linear systems, whereas blobs also receive nonlinear 'Y-like' M input.