Abstract

Considerable debate continues regarding thalamic inputs to the middle temporal area (MT) of the visual cortex that bypass the primary visual cortex (V1) and the role they might have in the residual visual capability following a lesion of V1. Two specific retinothalamic projections to area MT have been speculated to relay through the medial portion of the inferior pulvinar nucleus (PIm) and the koniocellular layers of the dorsal lateral geniculate nucleus (LGN). Although a number of studies have demonstrated retinal inputs to regions of the thalamus where relays to area MT have been observed, the relationship between the retinal terminals and area MT relay cells has not been established. Here we examined direct retino-recipient regions of the marmoset monkey (Callithrix jacchus) pulvinar nucleus and the LGN following binocular injections of anterograde tracer, as well as area MT relay cells in these nuclei by injection of retrograde tracer into area MT. Retinal afferents were shown to synapse with area MT relay cells as demonstrated by colocalization with the presynaptic vesicle membrane protein synaptophysin. We also established the presence of direct synapes of retinal afferents on area MT relay cells within the PIm, as well as the koniocellular K1 and K3 layers of the LGN, thereby corroborating the existence of two disynaptic pathways from the retina to area MT that bypass V1.

Highlights

  • According to current understanding, the dominant source of visual input to the middle temporal area (MT, V5), a ‘dorsal stream’ extrastriate area, comes from the primary visual cortex (V1), via the magnocellular retinogeniculocortical pathway (Born and Bradley, 2005)

  • Despite continued research, confirmation of the existence of disynaptic retinothalamic pathways to area MT is independent of the geniculostriate pathway has been thwarted by the inability to demonstrate synapses between cells of the specific component pathways

  • The concept of two parallel visual systems was originally developed by Diamond and colleagues (Snyder and Diamond, 1968) who ablated the striate cortex of the tree shrew and subsequently implied that a pathway to the visual temporal cortex parallel to the geniculostriate path capable of mediating visual discrimination in the absence of striate cortex must exist

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Summary

Introduction

The dominant source of visual input to the middle temporal area (MT, V5), a ‘dorsal stream’ extrastriate area, comes from the primary visual cortex (V1), via the magnocellular retinogeniculocortical pathway (Born and Bradley, 2005). Based on anatomical work two disynaptic retinothalamic pathways have been proposed to project to area MT in primates. One relays through the medial portion of the inferior pulvinar nucleus (PIm) (e.g. owl monkey, Lin and Kaas, 1980; squirrel and rhesus monkey, Cusick et al, 1993; macaque, Adams et al, 2000) which is the recipient of direct retinal projections (e.g. macaque, Cowey et al, 1994; O’Brien et al, 2001). The second relays through the koniocellular layers of the LGN (e.g. owl monkey, Stepniewska et al, 1999; macaque, Sincich et al, 2004; Nassi and Callaway, 2006), which is the recipient of direct retinal input in primates (e.g. macaque, Conley and Fitzpatrick, 1989; marmoset, Szmajda et al, 2008). To date, no evidence exists of direct synaptic connection of the two element pathways

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