Cortical Synaptic Arrangements of the Third Visual Pathway in Three Primate Species:Macaca mulatta, Saimiri sciureus, andAotus trivirgatus

Abstract

The koniocellular (K) pathway is one of three pathways from the lateral geniculate nucleus (LGN) to primate visual cortex (V1). K pathway projections to the cytochrome oxidase (CO) blobs of V1 suggest involvement in chromatic processing given reports that the CO blobs in diurnal primates contain cells selective for color. K LGN layers and CO blobs, however, are also well developed in nocturnal primates such as owl monkeys, which are likely to be color blind. Thus, the K pathway plays either different roles in different species or some as yet unidentified common role(s). Because synaptic arrangements underlie functional mechanisms, the purpose of this investigation was to compare the synaptic circuitry related to the K pathway within the CO blobs of two diurnal primates (macaque monkeys and squirrel monkeys) and one nocturnal primate (owl monkey). Presynaptic K axons were labeled with wheat germ agglutinin-HRP, and presynaptic and postsynaptic profiles in CO blobs were identified with post-embedding immunocytochemistry for GABA and glutamate. In all three species, K axon terminals are glutamatergic and larger than local axon terminals, suggesting that they have a greater impact on postsynaptic CO blob targets than signals arriving via layer IV from the P or M pathways. A greater proportion of K axons, however, synapse with larger glutamatergic shafts in the diurnal monkeys than in the nocturnal owl monkey, perhaps reflecting the importance of color within the K pathway of these diurnal species. Alternatively, the loss of color vision in the owl monkey could impact K pathway circuitry earlier in the pathway. The basic similarities between K axon circuitry within the CO blobs of the three primate species examined also could indicate that this pathway plays some common role or roles across species.

Neurochemical comparison of synaptic arrangements of parvocellular, magnocellular, and koniocellular geniculate pathways in owl monkey (Aotus trivirgatus) visual cortex

“…Above layer IV, distinct patchy label was seen within layer III with a central focus in sublayer IIIB␣. From our previous studies, we know that these patches of the label reflect the input from K LGN axons and that they coincide with the location of the CO blobs within this layer (Diamond et al, 1985;Casagrande, 1997, 1998;Shostak et al, 2002).…”

“…Studies of the synaptic circuitry of primate LGN input pathways have mainly examined M and P inputs to layer IV in macaque monkeys (Garey and Powell, 1971;Tigges and Tigges, 1979;Winfield and Powell, 1983;Freund et al, 1989). Only two studies have examined the synaptic circuitry of the K pathways in layer III CO-blobs (Ding and Casagrande, 1998;Shostak et al, 2002). These studies generally agree that M, P, and K axons mainly synapse with dendritic spines with a significant minority synapsing with dendritic shafts and very few synapsing with somata (Tigges and Tigges, 1979;Freund et al, 1989;Ding and Casagrande, 1998;Shostak et al, 2002).…”

“…Only two studies have examined the synaptic circuitry of the K pathways in layer III CO-blobs (Ding and Casagrande, 1998;Shostak et al, 2002). These studies generally agree that M, P, and K axons mainly synapse with dendritic spines with a significant minority synapsing with dendritic shafts and very few synapsing with somata (Tigges and Tigges, 1979;Freund et al, 1989;Ding and Casagrande, 1998;Shostak et al, 2002). No studies, however, have directly compared the synaptic arrangements made by all three classes of LGN axon in the same species.…”

“…No studies, however, have directly compared the synaptic arrangements made by all three classes of LGN axon in the same species. Also, few details are available concerning the neurochemical content of elements postsynaptic to primate LGN axons with the exception of K LGN axons (Garey and Powell, 1971;Tigges and Tigges, 1979;Winfield and Powell, 1983;Freund et al, 1989;Ding and Casagrande, 1998;Shostak et al, 2002).…”

“…We used the owl monkey for this study, both because its visual system is well studied (Casagrande and Kaas, 1994;O'Keefe et al, 1998;Xu et al, 2001) and because we have detailed knowledge from our own work on the termination and neurochemical synaptic arrangement of K axons in V1 Casagrande, 1997, 1998;Shostak et al, 2002).…”