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, 4C␣ and 4C␤, respectively, were intracellularly labeled, and their axonal and dendritic arbors were reconstructed. We find that neurons with dendrites in upper layer 4C␣ project axons to layer 4B and CO blobs in layer 2/3, thus relaying M input to these regions. Other neurons in lower layer 4C␣ provide M input to interblobs. These cells have either (1) dendrites restricted to lower layer 4C␣ and axons specifically targeting layer 2/3 interblobs, or (2) dendrites in lower 4C␣ and 4C␤ and axons targeting blobs and interblobs. P-recipient layer 4C␤ neurons have dense axonal arbors in both blobs and interblobs but not layer 4B. Quantitative analyses reveal that 4C␣ cells provide approximately five times more synapses than 4C␤ cells to layer 4B, whereas 4C␤ cells provide five times more synapses than 4C␣ 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 4C␣, not from afferents targeting only upper 4C␣ (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. Key words: functional streams; local circuits; macaque; primary visual cortex; primate; V1The relative contributions of the f unctionally distinct M and P pathways are believed to be important determinants of the functional differences between extrastriate cortical areas (Livingstone and Hubel, 1988; for review, see Merigan and Maunsell, 1993). Nevertheless, the actual relationships between the M and P streams and V1 neurons projecting to extrastriate cortex are poorly understood. We have addressed these relationships by studying spiny stellate neurons in layer 4C of V1, because they lie at the heart of the problem; they provide a direct link from LGN afferents to extrastriate projection neurons.In the retino -geniculo -cortical system, parallel M and P pathways converge on V1, where they segregate their inputs into layers 4C␣ and 4C␤, respectively (Hubel and Wiesel, 1972;Hen...

Oriented Axon Projections in Primary Visual Cortex of the Monkey

“…Neurons in layer 3 lie one synapse downstream from the geniculate-receptive layers 4C␤ and 4A, which have few cells with orientation selectivity (Hubel and Wiesel, 1968;Dow, 1974;Bullier and Henry, 1980;Blasdel and Fitzpatrick, 1984;Anderson et al, 1993;Ringach et al, 1997). Layer 4B, the intralaminar projections of which form the stria of Gennari, is also one synapse removed from its geniculate input in layer 4C␣ (Fitzpatrick et al, 1985;Yabuta and Callaway, 1998a). Layer 4B has a system of axon terminal patches lying in tight register with that in the upper layers (Fig.…”

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A Quantitative Map of the Circuit of Cat Primary Visual Cortex

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