Identification of a Pathway from the Retina to Koniocellular Layer K1 in the Lateral Geniculate Nucleus of Marmoset

Abstract

Three well characterized pathways in primate vision (midget-parvocellular, parasol-magnocellular, bistratified-koniocellular) have been traced from the first synapse in the retina, through the visual thalamus (lateral geniculate nucleus, LGN), to the visual cortex. Here we identify a pathway from the first synapse in the retina to koniocellular layer K1 in marmoset monkeys (Callithrix jacchus). Particlemediated gene transfer of an expression plasmid for the postsynaptic density 95-green fluorescent protein (PSD95-GFP) was used to label excitatory synapses on retinal ganglion cells and combined with immunofluorescence to identify the presynaptic bipolar cells. We found that axon terminals of one type of diffuse bipolar cell (DB6) provide dominant synaptic input to the dendrites of narrow thorny ganglion cells. Retrograde tracer injections into the LGN and photofilling of retinal ganglion cells showed that narrow thorny cells were preferentially labeled when koniocellular layer K1 was targeted. Layer K1 contains cells with high sensitivity for rapid movement, and layer K1 sends projections to association visual areas as well as to primary visual cortex. We hypothesize that the DB6-narrow thorny-koniocellular pathway contributes to residual visual functions ("blindsight") that survive injury to primary visual cortex in adult or early life.

Visual Functions of the Thalamus

“…Moreover, in contrast to neurons in the magnocellular and parvocellular layers, which have monocular responses, some neurons in the koniocellular layers have binocular responses (Cheong et al 2013), suggesting that individual koniocellular neurons combine retinal inputs either directly or through polysynaptic circuits. Finally, as evidence of the diversity of circuits that establish koniocellular responses, recent results have identified the full circuitry of a retinal pathway that supplies target neurons in the koniocellular layers with orientation and directional information, similar to that found in the mouse LGN (Cheong et al 2013, Percival et al 2014). …”

Survey of retinal ganglion cell morphology in marmoset

“…The images of labeled cells show brightly labeled puncta distributed along the dendritic tree (e.g., Figures c,f, e,h, f,h,j, and d). These puncta represent postsynaptic densities (Jakobs et al, ; Bleckert et al, ; Percival et al, ). Here, we analyzed a total of 574 ganglion cells.…”

“…Additional ganglion cell types project to the superior colliculus, the pretectum (Perry & Cowey, ; Rodieck, ; Rodieck and Watanabe, ; Dacey, Peterson, Robinson, & Gamlin, ), and the suprachiasmatic nucleus (Hannibal et al, ). Some or all of these cells also project to the LGN (Rodieck & Watanabe, ; Dacey, ), where they preferentially target the koniocellular layers (Szmajda et al, ; Percival, Martin, & Grünert, ; Percival, Koizumi, Masri, Buzas, Martin, & Grünert, ). Irrespective of their projections, these ganglion cells have dendritic fields larger than those of midget, parasol, and small bistratified cells and thus are collectively referred to as wide‐field cells (Peterson & Dacey, ; Yamada, Bordt, & Marshak, ).…”

Cellular and Circuit Mechanisms Shaping the Perceptual Properties of the Primate Fovea

“…The particles were delivered to retinal ganglion cells in whole-mount retinas using a Helios gene gun (Bio-Rad). Organotypic culturing and transfection of retinas was performed as described previously (Lye et al, 2007; Percival et al, 2014). In brief, pieces of retina were mounted ganglion cell side up onto a 0.4 μm Millicell tissue culture inset (Millipore).…”