During evolution, the primate cerebral cortex has expanded disproportionately, relative to overall brain size. Consequently, the cortical sheet becomes folded, to fit in the limited volume provided by the skull (Welker, 1990
). Inward-bending (concave) folds are called ‘sulci’, and outward-bending (convex) folds are called ‘gyri’. In a given species, the exact geometry of these folding patterns is not random (Sereno and Tootell, 2005
; Van Essen, 2007
); indeed it is consistent enough so that the major sulci and gyri are named individually (e.g. the calcarine sulcus, the superior temporal sulcus, the fusiform gyrus, etc.).
What determines these consistent folding patterns? Some developmental theories suggest that cortical folding is dictated by the differential growth of cortical layers (Richman et al., 1975
) or patterns of subcortical neurogenesis (Kriegstein et al., 2006
). An alternative theory has been proposed by Van Essen (1997)
: the mechanical tension along cortico-cortical connections is the primary driving force for cortical folding. The tension-based morphogenesis tends to reduce the aggregate length of axonal connections, thereby contributing to the compact wiring of neural circuitry in the brain.
In parallel, several groups have pointed out that the average length of cortical connections is also reduced by mapping adjacent retinotopic values along a common eccentricity value (e.g. Chklovskii and Koulakov, 2004
; Rajimehr and Tootell, 2007
); presumably this mechanism underlies the common ‘mirror symmetry’ in retinotopic areas V1, V2, V3, etc., and the ‘foveal patches’ (visual field map clusters) across visual cortex (Wandell et al., 2007
Collectively, these ideas suggest that the retinotopic organization may constraint the pattern of cortical folding in parts of visual cortex. Specifically, this hypothesis predicts that the border between adjacent, mirror-symmetric retinotopic areas (typically, the representation of the vertical meridian) would become a gyrus, and remaining regions of the retinotopic map (often including the horizontal meridian representation) would become sulci.
This hypothesis arises quite naturally from well-known details of the cortical architecture. In visual cortex, the retinotopic representation of the vertical meridian is unique because the vertical meridian forms the ‘seam’ between left versus right visual hemi-fields, which project to the right versus left hemispheres of the brain, respectively. Thus, the vertical meridian representation forms a single line across the cortical surface, dividing two adjacent, mirror-symmetric maps of the visual field. Corresponding retinotopic loci in each of these paired maps are strongly interconnected with each other, through short-range axons. However, loci along the vertical meridian are singularity points on the map of mirror-symmetric areas, so they lack these short-range, paired connections (connections from the vertical meridian are instead made via long-range callosal axons to the opposed hemisphere). During the development of cortical folds, relatively higher (and perhaps earlier) tension along these short-range axons would pull the paired retinotopic sites towards one another, resulting in a gyrus along the vertical meridian representation (which exercises less ‘pull’ on its own). By this idea, the horizontal meridian would tend to be driven into sulci as a secondary effect, because the horizontal meridian is furthest away from gyri defined by the vertical meridian. Additional effects may also contribute (see Discussion).
Qualitative support for this idea can be quite striking (see also Van Essen, 1997
). For instance in the macaque, the border between the most highly retinotopic areas (V1 and V2) is a vertical meridian representation that runs along the crown of two different gyri
(). Within the same areas, and the same range of visual field eccentricities, the horizontal meridian representations lie in and near two different sulci
(see ). A similar arrangement is found in V1 and V2 of human visual cortex (see ).
Representation of visual field meridians on folded and inflated cortex