Topographic organization of the “third tier” dorsomedial visual cortex in the macaque

Abstract

22The boundaries of the visual areas located anterior to V2 in the dorsomedial region of the 23 macaque cortex remain contentious. This region is usually conceptualized as including two 24 functional subdivisions: the dorsal component of area V3 (V3d), laterally, and another area, 25 named the parietooccipital area (PO) or V6, medially. However, the nature of the putative 26 border between V3d and PO/V6 has remained undefined. We recorded the receptive fields of 27 multiunit clusters in adult male macaques, and reconstructed the locations of recording sites 28 using histological sections and "unfolded" cortical maps. Immediately adjacent to 29 dorsomedial V2 we observed a representation of the lower contralateral quadrant, which 30 represented the vertical meridian at its rostral border. This region, corresponding to V3d of 31 previous studies, formed a simple eccentricity gradient, from approximately <5˚ in the 32 annectant gyrus, to >60° in the parietooccipital sulcus. However, there was no topographic 33 reversal where one would expect to find the border between V3d and PO/V6. Rather, near the 34 midline, this lower quadrant map continued directly into a representation of the peripheral 35 upper visual field, without an intervening lower quadrant representation that could be 36 unambiguously assigned to PO/V6. Thus, V3d and PO/V6 form a continuous topographic 37 map, which includes parts of both quadrants. Together with previous observations that V3d 38 and PO/V6 are both densely myelinated relative to adjacent cortex, and share similar input 39 from V1, these results suggest that they are parts of a single area, which is distinct from the 40 one forming the ventral component of the third tier complex. 41 42 Significance statement: The primate visual cortex has a large number of areas. Knowing the 43 extent of each visual area, and how they can be distinguished from each other, are essential 44 for the interpretation of experiments aimed at understanding visual processing. Currently, 45 there are conflicting models of the organization of the dorsomedial visual cortex rostral to 46 area V2 (one of the earliest stages of cortical processing of vision). By conducting large-scale 47 electrophysiological recordings, we found that what were originally thought to be distinct 48 areas in this region (dorsal V3, and the parietooccipital area [PO/V6]), together form a single 49 map the visual field. These results will help guide future functional studies, and the 50 interpretation of the outcomes of lesions involving the dorsal visual cortex. 51 Visual maps in macaque dorsomedial cortex 3 Introduction 52 53Despite four decades of research, there is still controversy regarding the boundaries of visual 54 areas in the "third tier" cortex, i.e., the areas located rostral to the second visual area (V2, 55 (Allman and Kaas, 1975). Here we focus on the parts of this complex located in the 56 dorsomedial region of the macaque brain, including the medial part of the lunate sulcus, 57 annectant gyrus, parietooccipital s...

Wide-field retinotopy reveals a new visuotopic cluster in macaque posterior parietal cortex

“…Figure 7 a–c show the average maps of pRF polar angle, eccentricity and size with the corresponding visuotopic parcellation on top of the right cortical hemisphere of the template monkey F99 (see Methods). Overall, we note a very good agreement between our observations and those of previous electrophysiological and imaging studies regarding the arrangement of upper/lower field representations in V3A/DP, V6/V6A and LIP (Galletti et al 1999a , b ; Hamed et al 2001 ; Arcaro et al 2011 ; Gamberini et al 2015 ; Hadjidimitrakis et al 2019a , b ). At the crossroad of these multiple visuotopic areas, we also note that the PIP cluster offers smooth visuotopic transitions thanks to its “cloverleaf” organization (Fig.…”

“…Concerning the lower visual field representations of PIP1 and PIP2 (“-” symbols), they face those of V3d posteriorly and V6/V6A medially. Overall, we note a very good agreement between our observations and those of previous electrophysiological and imaging studies regarding the arrangement of upper/lower field representations in V3A/DP, V6/V6A and LIP (Galletti et al 1999a , b ; Hamed et al 2001 ; Arcaro et al 2011 ; Gamberini et al 2015 ; Hadjidimitrakis et al 2019a , b ).

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“…Finally, the V6/V6A complex has been implied in the processing of visual motion, and our motion localizer clearly indicates the strong motion sensitivity of this cortical sector, as visible in Fig. 4 c. Medially, no clear demarcation between V3d and V6 could be delineated, confirming a recent report (Hadjidimitrakis et al 2019a , b ) of a continuous V3d/V6 eccentricity gradient. According to an older electrophysiological description of this boundary (Galletti et al 1999a , b ), no reversal in polar angle or eccentricity gradients is to be expected, compromising the ability to robustly identify this boundary based on polar angle or eccentricity maps alone.…”

“…In primates, the posterior parietal cortex (PPC) constitutes the end stage of the dorsal visual pathway and as such, it is notably involved in visuospatial and visuomotor functions (Buneo and Andersen 2006 ; Freedman and Ibos 2018 ; Hadjidimitrakis et al 2019a , b ). Most of what we know about how those functions are implemented in the PPC emanates from invasive (anatomical and electrophysiological) studies performed in macaque monkeys.…”

Receptor-driven, multimodal mapping of cortical areas in the macaque monkey intraparietal sulcus

“…However, a consensus has not yet been reached concerning the exact position of areas V3d and V3A in relation to the anectant gyrus. These discrepancies are probably due to the reported inter-individual variability in the width of area V3d ( Gattass et al, 1988 ; Gattass et al, 2005 ; Hadjidimitrakis et al, 2019b ) combined with the macroanatomical characteristics of this region of the macaque brain. Thus, depending on the relative width of area V3d, its border with V3A can be found either on the rostral wall of the anectant gyrus ( Lewis and Van Essen, 2000a ; Figure 13A ), on the apex of the gyrus ( Saleem and Logothetis, 2012 ; Figure 13B ), or on its posterior wall ( Nakamura et al, 2001 ; Ungerleider et al, 2008 ; Figure 13C ).…”