Retinotopic specializations of cortical and thalamic inputs to area MT

Abstract

Retinotopic specializations in the ventral visual stream, especially foveal adaptations, provide primates with high-acuity vision in the central visual field. However, visual field specializations have not been studied in the dorsal visual stream, dedicated to processing visual motion and visually guided behaviors. To investigate this, we injected retrograde neuronal tracers occupying the whole visuotopic representation of the middle temporal (MT) visual area in marmoset monkeys and studied the distribution and morphology of the afferent primary visual cortex (V1) projections. Contrary to previous reports, we found a heterogeneous population of V1-MT projecting neurons distributed in layers 3C and 6. In layer 3C, spiny stellate neurons were distributed mainly in foveal representations, while pyramidal morphologies were characteristic of peripheral eccentricities. This primate adaptation of the V1 to MT pathway is arranged in a way that we had not previously understood, with abundant stellate projection neurons in the high-resolution foveal portions, suggesting rapid relay of motion information to visual area MT. We also describe that the medial portion of the inferior pulvinar (PIm), which is the main thalamic input to area MT, shows a retinotopic organization, likely reflecting the importance of this pathway during development and the establishment of area MT topography.

Visual Cortical Area MT is Required for Development of the Dorsal Stream and Associated Visuomotor Behaviours

“…Further, since the monosynaptic V1-MT connection is yet to be fully established during this process, the early maturation of MT is thought to be independent of V1 input 4 . This knowledge, and the fact that MT has a first-order topographical map 5 and is directly recipient of thalamic connections 6,7 , supports the notion that it is a 'primary-like' area and serves as an anchor early in life to support establishment of the dorsal stream 8 .…”

“…In adulthood, MT receives significant input directly and indirectly from V1 5,9 , and is interconnected with multiple dorsal stream extrastriate areas, including V3 and the dorsomedial (DM) area, anterior and lateral intraparietal areas (AIP and LIP) [10][11][12][13] and the frontal eye fields (FEF) 14,15 (Fig 1a, b). Area MT also has abundant connections with subcortical structures, including reciprocal connections with the medial portion of the inferior pulvinar 4,7,16 , and afferent projections from the koniocellular layers of the lateral geniculate nucleus (LGN) 6 and superior colliculus 11,17,18 .…”

The Evolution of the Pulvinar Complex in Primates and Its Role in the Dorsal and Ventral Streams of Cortical Processing

“…The nucleus of the inferior pulvinar, that is densely interconnected with MT, is recognized as the medial nucleus of the inferior pulvinar (PIm). Both MT [12] and PIm [21] are retinotopically organized. The two bordering nuclei of the inferior pulvinar with dense inputs from the superior colliculus are the posterior nucleus of the inferior pulvinar (PIp) and the central medial nucleus of the inferior pulvinar (PIcm).…”

“…The nucleus that projects to MT, PIm, has few or no inputs from the superior colliculus and is activated instead by inputs from MT. Thus, PIm is more or less a satellite of MT, receiving inputs from MT and perhaps sending back a modulating input [42], although PIm receives some direct inputs from the retina [40,43], and the neurons projecting to MT appear to be drivers by being glutamatergic and weakly parvalbumin positive [21]. In intact monkeys, MT is highly dependent on V1 for activation (e.g., [44,45]), and lesions of the superior colliculus have no notable effect on the response properties of neurons in MT [46] nor on attention effects on MT neurons [47].…”

The postnatal development of MT, V1, LGN, pulvinar and SC in prosimian galagos (Otolemur garnettii)

“…In newborn galagos, PV is one of the best markers for area MT, as MT stains darkly for PV, and PV immunoreactivity is absent in surrounding areas (Figure b). This early postnatal PV labeling in MT (also see Mundinano et al, ) reflects axon terminations that are likely from the pulvinar (Mundinano, Kwan, & Bourne, ). Only a few cell bodies of neurons are labeled in MT at P3 (Figure a).…”