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Comparative Study
. 2009 Apr 8;29(14):4548-63.
doi: 10.1523/JNEUROSCI.0529-09.2009.

Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex

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Free PMC article
Comparative Study

Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex

Marcello G P Rosa et al. J Neurosci. .
Free PMC article

Abstract

The dorsomedial area (DM), a subdivision of extrastriate cortex characterized by heavy myelination and relative emphasis on peripheral vision, remains the least understood of the main targets of striate cortex (V1) projections in primates. Here we placed retrograde tracer injections encompassing the full extent of this area in marmoset monkeys, and performed quantitative analyses of the numerical strengths and laminar patterns of its afferent connections. We found that feedforward projections from V1 and from the second visual area (V2) account for over half of the inputs to DM, and that the vast majority of the remaining connections come from other topographically organized visual cortices. Extrastriate projections to DM originate in approximately equal proportions from adjacent medial occipitoparietal areas, from the superior temporal motion-sensitive complex centered on the middle temporal area (MT), and from ventral stream-associated areas. Feedback from the posterior parietal cortex and other association areas accounts for <10% of the connections. These results do not support the hypothesis that DM is specifically associated with a medial subcircuit of the dorsal stream, important for visuomotor integration. Instead, they suggest an early-stage visual-processing node capable of contributing across cortical streams, much as V1 and V2 do. Thus, although DM may be important for providing visual inputs for guided body movements (which often depend on information contained in peripheral vision), this area is also likely to participate in other functions that require integration across wide expanses of visual space, such as perception of self-motion and contour completion.

Figures

Figure 1.
Figure 1.
Results of electrophysiological recordings in animal CJ35, which received an injection of fluororuby in the location marked by the red “X”. Top left, Digital image of the surface of the brain obtained before the injection (medial is toward the top, rostral to the right; scale bar, 1 mm). This image was used to guide electrophysiological recordings conducted 2 weeks later. The colored circles indicate the location of electrode penetration sites, where receptive fields were mapped (at depths between 600 and 800 μm), and the dashed lines indicate our estimates of the borders of the upper (DM+) and lower (DM−) quadrant representations in DM. In V2 (fields 1–3), the receptive fields migrate toward the horizontal meridian of the visual field, as the electrode is moved rostrally. Crossing into DM, the sequence reverts toward the vertical meridian (fields 4–9). Moving from medial to lateral within DM, the receptive fields move from the lower visual field (e.g., fields 8–11), across the horizontal meridian (field 12), into the upper visual field (fields 13–17).
Figure 2.
Figure 2.
Main panel, Summary of current knowledge of the cortical organization in the marmoset, a New World monkey. “Unfolded” representation prepared using the technique of Van Essen and Maunsell (1980). Discontinuities in the representation, introduced to minimize distortion, are indicated by the arrows. The red, blue, and green asterisks represent corresponding points on two sides of a discontinuity. Continuous gray lines indicate the main cortical folds, including the lips and fundi of the lateral and calcarine sulci, the fundi of the superior temporal and intraparietal dimples, and the limits of the medial, ventral, and orbital surfaces. The inset on the lower left shows a lateral view of the intact marmoset brain, with boundaries of some visual areas indicated to help orientation. Colors indicate visual areas, with continuous outlines indicating borders that have been characterized in detail, and dotted lines indicating borders that are based on histology only. The topographic organization of visual areas is indicated according to the following symbols: black squares, representations of the vertical meridian; white circles, representations of the horizontal meridian; “+,” representations of upper quadrant; “−,” representations of the lower quadrant. Borders of nonvisual areas that are relevant for the present study are indicated by dotted outlines (primary sensory fields in dark gray), and the approximate location of other fields is indicated by their acronyms or numerical designations for orientation purposes only (for details, see Burman et al., 2006, 2008; Burman and Rosa, 2009). aud, Auditory belt and parabelt areas; ER, entorhinal cortex; Ins, insular cortex; PR, parietal rostral area; PV, parietal ventral area; som, caudal somatosensory areas; STP, superior temporal polysensory cortex. Upper left, Magnified view of the dorsomedial area, showing its visuotopic organization as mapped by Rosa and Schmid (1995). The lower quadrant, together with the entire periphery of the visual field, forms a continuous map in the medial portion of DM. A complementary sector of the visual field including the central part of the upper quadrant plus most of the upper vertical meridian, is “detached” from this map, being represented in the lateral part of DM. The blue stars indicate the line of visual field discontinuity in a typical animal (see Rosa et al., 2005 for details).
Figure 3.
Figure 3.
Myeloarchitectural characteristics of cortical areas of the marmoset (Gallyas stain). Transition zones between areas are indicated by lines overlying the cortex, and their centers by overlying arrows. In the lower panel, the extent of the main subdivisions of the posterior parietal cortex (PPd and PPv) is indicated by the arrowheads underlying layer 6. As discussed in Materials and Methods, these contain multiple subfields (including MDP, PEc, VIP, LIP, PF, and TPt, which are visible in this illustration).
Figure 4.
Figure 4.
Series of parasagittal sections (A–F) showing the location of FR-labeled neurons (red) in case CJ35-FR (rostral to the right). The centers of the transition zones between areas are indicated by blue lines across the cortex. The levels of these sections are indicated in the inset (upper left), which is a two-dimensional reconstruction of the cortex in this case, prepared using the conventions shown in Figure 2. The locations of a few cortical areas [V1, V2, DM, MT, and the primary somatosensory area (S1)] are indicated in gray for orientation. The detailed map of distribution of label in this case is illustrated in Figure 5. Scale bars, 1 mm. Abbreviations for subcortical structures are as follows: Cel/CeM, central lateral/central medial thalamic nuclei; Cla, claustrum; Pul, pulvinar complex.
Figure 5.
Figure 5.
Distribution of label after a tracer injection in DM (case CJ35) (see also Figs. 1, 4). The main panel shows an unfolded representation of the right hemisphere, prepared in the style shown in Figure 1, with the injection site shown in concentric black (core) and white (halo) zones. Thick solid lines indicate the main cortical folds such as the lateral, intraparietal, calcarine, and superior temporal sulci, and the limits between the medial, dorsal, ventral, and orbital surfaces. Histological transition zones between areas are indicated in semitransparent gray, and estimated borders (i.e., borders that could not be visualized directly in this case, but were drawn based on previous results in other animals) are shown in dotted gray lines. To help visualize the borders of DM in regions of dense label, the myeloarchitectural transition zone of this area is highlighted with thin dark lines. The number of labeled cells within 400 × 400 μm regions is indicated as a percentage of the maximum value using the color scale shown on the bottom right (maximum count in this case: 15 cells per unit area). The total number of cells counted in this case was 4158. Scale bar, 2 mm. The red dashed line overlying the V1 map indicates an estimate of the boundary between the upper (V1+) and lower (V1−) quadrant representations. The inset on the top left indicates the visuotopic extent of the injection site, as projected to a diagram of the contralateral hemifield (numbers indicate eccentricities; black lines indicate the limits of the left hemifield; VM, vertical meridian; HM, horizontal meridian). In this diagram the red region encompasses the region estimated by the location of labeled cells in V1 (red), and the white rectangles correspond to the receptive fields recorded closest to the injection site.
Figure 6.
Figure 6.
Distribution of label after an injection of DY in the representation of the upper visual quadrant in DM. The borders of DM near the injection site are indicated by the thick dark dashed line. Total count = 3227 cells, maximum = 25 cells per unit area. Other conventions are as in Figure 5.
Figure 7.
Figure 7.
Distribution of label after an injection of FR in the representation of the upper visual quadrant in DM. Total count = 2351 cells, maximum = 20 cells per unit area. Conventions are as in Figure 5.
Figure 8.
Figure 8.
Distribution of label after a FB injection in caudal DM, which involved the upper and lower quadrant representations. Total count = 8085 cells, maximum = 41 cells per unit area. Conventions are as in Figure 5.
Figure 9.
Figure 9.
A, Distribution of label after a FB injection in rostral DM, which was centered in the central (5°) representation of the lower quadrant, but also involved the representation of the peripheral upper quadrant. Total count = 4549 cells, maximum = 20 cells per unit area. B, In this same animal, a DY injection was placed in area MT. Total count = 16,268 cells, maximum = 64 cells per unit area. In each panel, the regions where labeled cells may have been obscured by the other injection site are indicated as gray ovals. Other conventions are as in Figure 5.
Figure 10.
Figure 10.
Distribution of label after a small injection of FE in the representation of the lower visual quadrant in DM. Total count = 3054 cells, maximum = 22 cells per unit area. Conventions are as in Figure 5.
Figure 11.
Figure 11.
Distribution of label after an injection of FE along the portion of DM located on the midline cortex, which labeled primarily the representation of the lower visual quadrant in DM, but crossed slightly into the representation of the peripheral upper quadrant. Total count = 3574 cells, maximum = 15 cells per unit area. Conventions are as in Figure 5.
Figure 12.
Figure 12.
Distribution of label after an injection of FE in the most rostral portion of DM, which involved both the dorsal surface and midline cortices. This injection, which corresponded to the representation of the peripheral lower visual quadrant in DM, crossed slightly into the cortical area immediately rostral to DM (PPm), leading to additional labeled regions in the frontal and parietal regions. Note also the increased label in the retrosplenial cortex (area 23v), which is typically only found after injections in the far peripheral representations of extrastriate cortex (Palmer and Rosa, 2006b). Total count = 2467 cells, maximum = 13 cells per unit area. Conventions are as in Figure 5.
Figure 13.
Figure 13.
Percentages of labeled neurons located in different cortical subdivisions after injections in DM. Data from six animals are illustrated, with the bars arranged approximately in central to peripheral sequence. The abbreviation GFC represents all label located in the granular frontal cortex. See also Table 2. FC, Frontal cortex.
Figure 14.
Figure 14.
Percentage of supragranular layer neurons (%SLN) in the projections from different cortical areas and regions to DM. Data from six injections are illustrated, using the same conventions as in Figure 13. See also Table 2.
Figure 15.
Figure 15.
Summary of the results of quantitative analyses of the cortical afferents of DM. The boxes representing each area or region containing labeled cells were arranged vertically according to the %SLN observed in the different projections to DM. The thickness of each connecting line is indicative of the numerical strength of the projections (strongest projections corresponding to the thickest lines).

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