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

ABSTRACT

As in other primates, the lateral geniculate nucleus (LGN) of owl monkeys contains three anatomically and physiologically distinct relay cell classes, the magnocellular (M), parvocellular (P), and koniocellular (K) cells. M and P LGN cells send axons to the upper and lower tiers of layer IV, and K cells send axons to the cytochrome oxidase (CO) blobs of layer III and to layer I of primary visual cortex (V1). Our objective was to compare the synaptic arrangements made by these axon classes. M, P, and K axons were labeled in adult owl monkeys by means of injections of wheat germ agglutinin-horseradish peroxidase into the appropriate LGN layers. The neurochemical content of both pre- and postsynaptic profiles were identified by postembedding immunocytochemistry for gamma-aminobutyric acid (GABA) and glutamate. Our key finding is that the synaptic arrangements made by M, P, and K axons in owl monkey exhibit more similarities than differences. They are exclusively presynaptic, contain glutamate and form asymmetric synapses mainly with glutamate-positive dendritic spines. The majority of the remaining axons synapse with glutamatergic dendritic shafts. There are also differences between LGN pathways. M and P terminals are significantly larger and more likely to make multiple synapses than K axons, although M and P axons do not differ from each other in either of these characteristics. Of interest, a larger percentage of M and K axons than P axons make synapses with GABAergic dendritic shafts. Cells directly postsynaptic to M and K axons are known to exhibit orientation selectivity and, in some cases, direction selectivity. Cells postsynaptic to P axons do not show these properties, but instead tend to reflect their LGN inputs more faithfully; therefore, it is possible that these physiologic differences seen in the cortical cells postsynaptic to different LGN pathways reflect the differential involvement of inhibitory circuits.