Retinal afferents synapse with relay cells targeting the middle temporal area in the pulvinar and lateral geniculate nuclei

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.

The Early Maturation of Visual Cortical Area MT is Dependent on Input from the Retinorecipient Medial Portion of the Inferior Pulvinar

“…Previous studies have demonstrated the presence of two monosynaptic pathways from the pulvinar nucleus and LGN to area MT in adult nonhuman primates (Lin and Kaas, 1980;Cowey et al, 1994;Adams et al, 2000;O'Brien et al, 2001;Warner et al, 2010), but none have examined when they are present and whether they change during development. Therefore, injection of the retrograde tracer FB into area MT (Fig.…”

“…The previously described retinofugal pathways to area MT via the koniocellular (K) layer of the lateral geniculate nucleus (LGN) (Sincich et al, 2004) and medial portion of the inferior pulvinar nucleus (PIm) (Sincich et al, 2004;Lyon et al, 2010;Warner et al, 2010) are likely candidates (Fig. 1).…”

Unravelling the development of the visual cortex: implications for plasticity and repair

“…1) (Felleman & Van Essen, 1991). The innervation of the visual cortex by the thalamus is also highly segregated in the primates, with the lateral geniculate nucleus (LGN) specifically innervating V1, and the other visual thalamic nuclei such as the pulvinar innervating extrastriate areas such as the MT area (Sincich et al 2004;Lyon et al 2010;Warner et al 2010). The discovery and analysis of visual cortical areas in the human and non-human primates have been a major accomplishment in visual neuroscience, and the location, number and functional roles of the individual nuclei are major topics of investigation in the adult and developing brain.…”

“…Furthermore, this has been recently enhanced with an increased number of fluorescent-conjugated tracers (e.g. B-subunit cholera toxin) (Warner et al 2010;Angelucci et al 1996;Behrens et al 2003), and complex transneuronal tracers including the neurotropic (rabies) viruses used by Edward Callaway and colleagues in macaque monkeys , 2007, which can be produced to cross a predetermined number of synapses in the visual system. Although tracer studies are limited primarily to studies in experimental animals, new techniques in magnetic resonance imaging (MRI) such as diffusion tensor imaging (which measures the restrictions on water along nerve fibre bundles) has shown potential in enabling the mapping of thalamocortical and corticocortical connectivity (Behrens et al 2003;Hagmann et al 2003;Dauguet et al 2007;Bridge et al 2008), and although there are specific limitations with this technique, it has become an invaluable resource for studying both the intact and damaged human brain.…”

“…One relays through the medial portion of the inferior pulvinar nucleus (PIm) [e.g. owl monkey (Lin & Kaas, 1980), squirrel and rhesus monkey (Cusick et al 1993), macaque (Adams et al 2000), marmoset (Warner et al 2010)]. The second relays through the koniocellular layers of the LGN [e.g.…”