High-Resolution Mapping of Anatomical Connections in Marmoset Extrastriate Cortex Reveals a Complete Representation of the Visual Field Bordering Dorsal V2

Abstract

The primate visual cortex consists of many areas. The posterior areas (V1, V2, V3, and middle temporal) are thought to be common to all primate species. However, the organization of cortex immediately anterior to area V2 (the "third tier" cortex) remains controversial, particularly in New World primates. The main point of contention has been whether the third tier cortex consists of a single area V3, representing lower and upper visual quadrants in dorsal and ventral cortex, respectively, or of 2 distinct areas (the dorsomedial [DM] area and a V3-like area). Resolving this controversy is crucial to understand the function and evolution of the third tier cortex. We have addressed this issue in marmosets, by performing high-precision mapping of corticocortical connections in cortex bordering dorsal V2. Multiple closely spaced neuroanatomical tracer injections were placed across the full width of dorsal V2 or adjacent anterior cortex, and the location of resulting labeled cells mapped throughout whole flattened visual cortex. The resulting topographic patterns of labeled connections allowed us to define areas and their boundaries. We found that a complete representation of the visual field borders dorsal V2 and that the third tier cortex consists of 2 distinct areas. These results unequivocally support the DM model.

The case for a dorsal V3 in the ‘third-tier’ of primate visual cortex: a reply to ‘the case for a dorsomedial area in the primate ‘third-tier’ visual cortex’

“…7 of Jeffs et al [24] (see fig. 8 as well) a V3d pattern is actually visible if one uses a smaller 2.5 or 3 mm estimate of the width of V2.…”

“…An overestimate of the outer border of dorsal V2 will result in a larger V2 that effectively consumes V3d within it, leading to the interpretation that V3 is not present. Thus, the difference in interpretation is not due to the fact that only four to five tracers were used for our injections into marmoset V1 [16] and up to seven tracers were used in V2 by Jeffs et al [24], it is rather that we interpret the outer border of V2 to be in a relatively different location, rostrocaudally. The provided CO stains in Jeffs are particularly useful for determining the V1/V2 border and the MT/MTc complex [24].…”

“…Thus, the difference in interpretation is not due to the fact that only four to five tracers were used for our injections into marmoset V1 [16] and up to seven tracers were used in V2 by Jeffs et al [24], it is rather that we interpret the outer border of V2 to be in a relatively different location, rostrocaudally. The provided CO stains in Jeffs are particularly useful for determining the V1/V2 border and the MT/MTc complex [24]. However, in their examples, it is difficult to identify with much certainty the outer border of V2; this border largely seems to be estimated and is much larger at the widest portion of dorsal V2, approximately 4 mm in their fig.…”

“…In summary, it seems likely that differences in the localization of the outer border of dorsal V2 is the primary reason for the very different conclusions regarding V3d and DM following the analysis of connection patterns [6][7][8]16,24]. Even while more anatomical studies would certainly help in evaluating whether or not there is a DM or a V3d immediately adjacent to the outer border of dorsal V2, the preponderance of evidence from imaging of retinotopic maps in monkeys and humans [1] is overwhelmingly in favour of V3d.…”

The case for a dorsomedial area in the primate ‘third-tier’ visual cortex

“…However, we disagree with the conclusions of Lyon & Connolly regarding the location and extent of this area. Here, we argue that studies which mapped in detail the receptive fields (RFs) [1,5,6] and anatomical connections [4,7] of cortex immediately rostral to the dorsal half of V2, particularly in New World monkeys, demonstrate the existence of a dorsomedial area (DM) in this location. According to this scheme, a V3-like area, which is less extensive than that proposed by Lyon & Connolly, occupies only the lateral and ventral aspects of the third-tier cortex.…”