Topographic organization in the brain: searching for general principles

Abstract

The neurons comprising many cortical areas have long been known to be arranged topographically such that nearby neurons have receptive fields at nearby locations in the world. Although this type of organization may be universal in primary sensory and motor cortex, in this review we demonstrate that associative cortical areas may not represent the external world in a complete and continuous fashion. After reviewing evidence for novel principles of topographic organization in macaque lateral intraparietal area (LIP) - one of the most-studied associative areas in the parietal cortex - we explore the implications of these new principles for brain function.

Figure 1

Retinotopic organization of macaque visual cortex from [54]. A) The legend demonstrates the organization of the visual field in polar coordinates. The dotted lines delineate eccentricity contours with the dark triangles marking the visual periphery. The polar angle coordinates are bounded by meridians that are represented by the dark squares (horizontal meridian), + symbols (upper field vertical meridian), and − symbols (lower field vertical meridian). The eccentricity coordinates are bounded by the triangles, and smaller eccentricities are represented by the dashed lines. B) Flattened schematic representation of visual cortical areas, with simulated coordinates from A) mapped onto each visual area. Note that the represented visual field covers the entirety of each of the visual areas, and that all portions of each visual hemifield are represented in each visual area, even if the area (such as V2) is separated into discontinuous parts.

Figure 2

Anatomy of LIP. A) Dorsal/posterior/lateral view of inflated right hemisphere. B) Coronal sections through LIPv (red) and LIPd (yellow). C) Flattened right hemisphere with tracings (blue) of lateral bank of the IPS from each of the slices in B. Figures A–C on F99 macaque atlas [83], LIPv and LIPd from [46] atlas. D) LIPv and LIPd (black outlines) can be distinguished by their myelin content, shown here on YerkesMacaque19 atlas [84].

Figure 3

Topographic organization of LIP from five studies. Data transferred to flattened segment of F99 macaque atlas, with LIPv and LIPd borders from [46]. For Patel et al. the data were directly projected from the F6 atlas used in the study to the F99 surface. In the two other imaging studies (Figures 3C–E), the data alignment was approximated by matching anatomical markers such as the fundus of the IPS with the F99 surface. In the single-unit recording studies (Figures 3A and B), alignment was achieved by matching the illustrated coronal sections to the coronal sections of the F99 macaque atlas, and used these aligned slices to anchor the projections to the F99 surface. Because of potential scale differences between the two species (and between fixed versus in vivo brains) we relied more heavily on anatomical features than stereotaxic coordinates. Primary colors represent stimulation in the upper (red) or lower (blue) visual fields or at the horizontal meridian (green). Light blue represents stimulation at fixation or at the fovea, orange represents parafovea (<7° eccentricity), lighter polar angle colors 7°–15° eccentricity, and darker colors >15° eccentricity.

Figure 4

Possible topographically-organized hand representations. A) Schematic of minimally distorted, topologically intact hand representation. Color gradient indicates dorsal/ventral surface locations on digits (D₁-D₅) from distal (red) to proximal (green). B) Schematic of actual topographically-discontinuous hand representation found in somatosensory cortex. Color gradient indicates locations on ventral digit surfaces from D₅ (red) to D₁ (green). C) Hand representation in somatosensory areas 3b and 1 of the owl monkey (adapted from [85]).

Figure 5

Possibilities for LIP topographic organization. A) Separate maps for attention and saccades. B) Overlapping attention and saccade maps.