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The Journal of Neuroscience, December 6, 2006, 26(49):12789-12798; doi:10.1523/JNEUROSCI.4044-06.2006

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Behavioral/Systems/Cognitive
Multiple Circuits Relaying Primate Parallel Visual Pathways to the Middle Temporal Area

Jonathan J. Nassi and Edward M. Callaway

Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, La Jolla, California 92037

Correspondence should be addressed to Edward M. Callaway, Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: callaway{at}salk.edu

Parallel pathways in the primate visual system parse the sensory signal into magnocellular (M), parvocellular (P), and koniocellular (K) streams. These pathways remain anatomically separate and distinct from their origination in different retinal ganglion cell types, through distinct layers of the lateral geniculate nucleus, and into primary visual cortex (V1), with the M pathway terminating primarily in layer 4C, the P pathway in layer 4Cß, and the K pathway in the cytochrome oxidase blobs of layer 2/3. Recent studies indicate that outputs from V1 are less compartmental than previously thought, making it difficult to assess the contributions of M and P pathways to areas beyond V1 in the dorsal and ventral streams. Here we use rabies virus as a retrograde transsynaptic tracer to study the contributions of M and P pathways to areas middle temporal (MT), V3, and V2 of macaque monkey. We find that, although disynaptic inputs through layer 4C of V1 to dorsal stream area MT are dominated by the M pathway, within an additional three synapses MT receives a substantial P input. This P input is unlikely to reach MT via V3, which we show also receives disynaptic inputs dominated by the M pathway. We find that disynaptic inputs to V2, however, can be more balanced and may carry convergent M and P input to MT. Our observations provide evidence for multiple pathways from V1 to MT, with varying degrees of M and P convergence. Each pathway likely provides functionally specialized information to MT and dorsal stream visual processing.

Key words: macaque; vision; retrograde labeling; transsynaptic; rabies virus; primary visual cortex; magnocellular; parvocellular

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Received Sept. 15, 2006; revised Oct. 27, 2006; accepted Nov. 1, 2006.

Correspondence should be addressed to Edward M. Callaway, Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: callaway{at}salk.edu

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