Resolving the organization of the third tier visual cortex in primates: A hypothesis-based approach

Abstract

As highlighted by several contributions to this special issue, there is still ongoing debate about the number, exact location, and boundaries of the visual areas located in cortex immediately rostral to the second visual area (V2), i.e., the “third tier” visual cortex, in primates. In this review, we provide a historical overview of the main ideas that have led to four models of third tier cortex organization, which are at the center of today’s debate. We formulate specific predictions of these models, and compare these predictions with experimental evidence obtained primarily in New World primates. From this analysis, we conclude that only one of these models (the “multiple-areas” model) can accommodate the breadth of available experimental evidence. According to this model, most of the third tier cortex in New World primates is occupied by two distinct areas, both representing the full contralateral visual quadrant: the dorsomedial area (DM), restricted to the dorsal half of the third visual complex, and the ventrolateral posterior area (VLP), occupying its ventral half and a substantial fraction of its dorsal half. DM belongs to the dorsal stream of visual processing, and overlaps with macaque parietooccipital (PO) area (or V6), whereas VLP belongs to the ventral stream and overlaps considerably with area V3 proposed by others. In contrast, there is substantial evidence that is inconsistent with the concept of a single elongated area V3 lining much of V2. We also review the experimental evidence from macaque monkey and humans, and propose that, once the data are interpreted within an evolutionary-developmental context, these species share a homologous (but not necessarily identical) organization of the third tier cortex as that observed in New World monkeys. Finally, we identify outstanding issues, and propose experiments to resolve them, highlighting in particular the need for more extensive, hypothesis-driven investigations in macaque and humans.

A new view of dorsal visual cortex in macaques revealed by submillimeter fMRI

“…Although not immediately apparent, this New World monkey model could be compatible with the macaque data, since the upper quadrant of V3A in macaque model 1 can be combined with the most medial part of V3d and PO/V6 to form a DM-like region as in macaque model 2 ( Figure 1D). Moreover, the lowerquadrant representation assigned to V3A in macaque model 1 resembles the LVF representation of VLP (VLP-) in the New World monkey model ( Figure 1D) (Angelucci and Rosa, 2015;Rosa and Tweedale, 2005).…”

“…A putative New World marmoset model also requires merging R2-(DLP-) with V3v, since V3v alone would then constitute an improbable area in which only one quadrant is represented (Angelucci and Rosa, 2015;Rosa and Tweedale, 2000a;. R2 (DLP) contains the same mirror image representation of the visual field as V3v, however, its receptive field size is significantly larger than V3v.…”

“…The visuotopic organization of third-tier visual areas in macaque monkeys has been a longstanding source of controversy, even ~40 years after their discovery (Angelucci and Rosa, 2015;Gattass et al, 2015;Jeffs et al, 2015;Kaas et al, 2015;Sereno et al, 2015). Different visuotopic representations have been described immediately rostral to the secondary visual area (V2), leading to a profusion of partitioning models for the third visual area V3 (Figure 1).…”

A twisted visual field map in the primate cortex predicted by topographic continuity

“…First, a "twist" in visual field topography, leading to sectors of mirror-and non-mirror representation within a single area; and second, regions of rapid change in receptive field position within the map, which bridge the transition between mirror-and non-mirror sectors. Using unbiased, high-resolution maps of the controversial dorsal extrastriate region 14,15 we then demonstrate that this type of map actually exists in the visual cortex of a non-human primate (the marmoset). This demonstrates that even under simple wiring principles, the resulting topography of cortical maps can be complex, and suggests that robust parcellation of the visual cortex requires a more detailed analysis than that afforded by any single metric such as field sign.…”

“…2a) 17 . However, this proposal was based on qualitative evidence, and the available data also led to other models according to which the same region contains areas with more conventional retinotopy 8,14,15 .…”