Research ArticleNEUROSCIENCE

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

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Science Advances  28 Oct 2020:
Vol. 6, no. 44, eaaz8673
DOI: 10.1126/sciadv.aaz8673
  • Fig. 1 A model for retinotopic map formation in the extrastriate cortex.

    (A) Schematic of early visual areas on flat-mounted cortex. The green rectangle represents the cortical region whose retinotopy was learned by the model (area “DM”). Landmarks of the visual field (upper/lower field, meridians, and center of gaze) are represented by symbols depicted in the inset. V1 and V2 are shaded by their field signs (dark red, mirror image; dark blue, nonmirror image). (B) DM neurons in the model are represented by open circles arranged in a grid (rows are illustrated with horizontal red lines, and columns with vertical blue lines). Receptive field locations are constrained by within-area smoothness (purple arrows) and between-area congruence (green arrows). The latter constraint operates among neighboring DM and V2d neurons (filled circles). (C) One particular retinotopy produced by the model, visualized as the cortical grid projected to the visual space. As in (B), rows of neurons are connected by red lines, and columns by blue lines. (D) The same retinotopy visualized in the cortical space, where each node of the grid is shaded with a color representing the polar angle of its receptive field (the color scale is illustrated in Fig. 2B). The eccentricities of the receptive fields are visualized with dashed white contours. V1d/v, the dorsal and the ventral part of the primary visual area; V2d/v, the dorsal and the ventral part of the secondary visual area; DM, the dorsomedial visual area; VM, vertical meridian; HM, horizontal meridian; C, caudal; R, rostral; M, medial.

  • Fig. 2 The dependency between the developed retinotopy and the modeling parameters.

    (A) Conventional retinotopy produced by the model; colors represent polar angle, and dashed white contours represent eccentricity. (B) Field sign at each location. (C) The progression of receptive field locations, if they are sampled on a path in the direction indicated by the blue arrow in (A). (D) The same map as in (A), illustrated in visual space. (E to H) A “twisted” retinotopy produced by the model. (I) The relationship between the two parameters and the field sign of the resulting map. The gray scale indicates field sign homogeneity (λ¯ = 0, balanced mirror and nonmirror image field sign; λ¯ = 1, mirror image field sign). Regions indicated by “A,” “B,” and “C” correspond to the three types of maps illustrated in the bottom row.

  • Fig. 3 Quantitative receptive field mapping (case CJ138).

    (A) Receptive fields for all active channels in the 10 × 10 multielectrode array were mapped with a flashing square stimulus displayed on randomized locations. The color scale represents the magnitude of the evoked responses. The cross-hair inside each map represents the estimated HM and VM. (B) Coordinates of the receptive fields were extracted. The eccentricity map was generated by interpolation and smoothing. (C) So was the polar angle map. (D) The gradients of eccentricity and polar angle were estimated for field sign calculation. (E) Boundaries of areas were identified. The retinotopic maps are illustrated in the same formats as in Fig. 3.

  • Fig. 4 High-resolution retinotopy of the dorsomedial cortex.

    (A) Schematic summary of one of the models of the organization of dorsomedial cortex in the marmoset (16). The inset at the bottom right illustrates the color scheme used to illustrate different segments of the visual hemifield in the proposed area DM. The arrow indicates the location of the putative map discontinuity. (B) Retinotopy of five hemispheres from four animals (identifiers of the cases are prefixed by “CJ”), estimated from the quantitative procedure illustrated in Fig. 3. The color scale represents polar angles. Polar angle contours are indicated by solid black contours and numbers in black. Eccentricities are indicated by dashed white lines and numbers in white. Inset: The color scale for representing polar angles in (B) and (C). The HM (polar angle = 0°) is indicated by thick lines overlaid with circles. The VM (polar angle ±90°) is indicated by thick lines and squares. (C) Composite summary of the spatial relationships shown in (B) based on array implantation sites identified on histological sections (fig. S6). V1, primary visual area; V2d, dorsal portion of secondary visual area; DM+/DM−, upper/lower field representation of the dorsomedial (DM) area; DA, dorsoanterior area; DI, dorsointermediate area.

  • Fig. 5 Unusual features of DM retinotopy and field sign summaries.

    (A) Eccentricity maps of two selected cases. (B) Maps of partial gradient of eccentricity with respect to the medial-lateral axis (y axis) of the electrode arrays. The regions shaded in a blue color scale (enclosed by the orange contours) correspond to sites where the eccentricity of the receptive field rapidly decreased in the lateral-to-medial direction. The contours are duplicated in (A). (C) Representative sequences of receptive fields associated with channels in columns of the electrode arrays. The association between the receptive fields and the channels is identified by letters (columns) and numbers (rows). In these plots, receptive field locations were not smoothed across channels. (D) Summary of the field signs for areas in the dorsomedial region of the marmoset visual cortex. The field signs for areas DM, DI, VLP (or V3), and VLA (or V4) were inferred from published maps (26). (E) Field sign maps estimated for the five cases. The locations of the arrays were established by histological examination of flat-mounted sections and visualization of the arrays relative to the borders of V1 and V2 (see fig. S6). VLP, ventrolateral posterior area; VLA, ventrolateral anterior area.

  • Fig. 6 Modeling different scenarios of map formation in the early visual cortex.

    (A) Schematic illustration showing the spatial relationships among the three modeling scenarios whose results are shown in (B) (indicated by the cyan rectangle), (C) (indicated by the purple rectangle), and (D) (indicated by the pink rectangle). (B) Retinotopy map (left) and the field sign map (right) developed in a configuration similar to area V2. The maps are displayed in the same format as in Fig. 2. The β1 and β2 parameters were set to (0.04, 0.04). (C) Retinotopy developed in a configuration similar to the traditional view of V3. (β1, β2) = (0.123 0.123). (D) Retinotopy developed if an area with a dimension similar to DM was displaced to be adjacent to the foveal representation of V2. (β1, β2) = (0.05 0.05). Additional details about the simulation are provided in fig. S5.

Supplementary Materials

  • Supplementary Materials

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

    Hsin-Hao Yu, Declan P. Rowley, Nicholas S. C. Price, Marcello G. P. Rosa, Elizabeth Zavitz

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