Adaptive Pulvinar Circuitry Supports Visual Cognition

Abstract

The pulvinar is the largest thalamic nucleus in primates and one of the most mysterious. Endeavors to understand its role in vision have focused on its abundant connections with the visual cortex. While its connectivity mapping in the cortex displays a broad topographic organization, its projections are also marked by considerable convergence and divergence. As a result, the pulvinar is often regarded as a central forebrain hub. Moreover, new evidence suggests that its comparatively modest input from structures such as the retina and superior colliculus may critically shape the functional organization of the visual cortex, particularly during early development. Here we review recent studies that cast fresh light on how the many convergent pathways through the pulvinar contribute to visual cognition.

Keywords: human; primate; superior colliculus; thalamus; vision; visual cortex.

Figure 1. Connectivity of the pulvinar subregions

The pulvinar has significant reciprocal connectivity with the cortex, here summarized in cartoon form with lines depicting bidirectional connections except the connections from the retina and superior colliculus (SC), which are unidirectional. Hatched lines indicate reported connections that are controversial or have not been verified. Specific subdivisions within the inferior pulvinar (PI) and lateral pulvinar (PL) send and receive projections from both dorsal and ventral streams of the visual cortex. The medial subdivision of the inferior pulvinar (PIm) is recipient of input from the retina, and a disputed input from the superior colliuculus (SC; hatched line). The PIm in turn relays to the middle temporal (MT) area, the medial superior temporal area (MST) and the fundus of the superior temporal area (FST); all components of the dorsal stream. The central medial (cm) and posterior (p) subdivisions of the PI also connect with dorsal stream areas MST, FST and the crescent of the middle temporal area (MTc). The central lateral subdivision of the PI (PIcl) and the ventrolateral (vl) subdivision of PL are heavily connected with the ventral stream associated areas V1, V2, V3 and V4. Other subdvisions have indirect connectivity with the visual cortex. The dorsal medial (dm) subdivision of PL projects to the inferior parietal cortex and the dosolateral prefrontal cortex (DLPFC). The medial pulvinar (PM), which possesses a lateral (l) and medial (m) subdivision projects to the temporal and parietal cortex, while the PMm also projects to the DLPFC, orbitofrontal cortex (OFC) and amygdala. The PM has been suggested to be recipient of input from the SC (hatched line), as has the PL

Figure 2. The developmental trajectory of the retino-pulvinar-MT pathway and the effects of early-life damage to V1

A: In the marmoset neonate, a prominent direct pathway (blue arrow) carries retinal information through the optic tract (OT) to the medial division of the inferior pulvinar (PIm), in addition to the lateral geniculate nucleus (LGN). A thalamocortical pathway from PIm (red arrow) is thought to pass this image information to cortical area MT, thus completing the early visual pathway to the extrastriate cortex. B: During normal development, as the LGN pathway matures and begins to dominate visual input to the cortex through the optic radiations (OR), the early visual pathway through PIm regresses. C: When animals develop in the context of an early life V1 lesion, this regression fails to occur. The LGN undergoes significant degeneration and both the afferent and efferent components of the PIm visual pathway remain intact. It may be for this reason that early life V1 lesions lead to a significant retention of vision. However, following a lesion of V1 in adulthood (not shown), the degeneration of the LGN is not accompanied by a strenghtening of the PIm-MT pathway, which has already regressed. Thus subjects with adult V1 lesions experience blindness.