Topological Singularities in Cortical Orientation Maps: the Sign Theorem Correctly Predicts Orientation Column Patterns in Primate Striate Cortex

Optical imaging methods have revealed the spatial arrangement of orientation columns across striate cortex, usually summarized in terms of two measurements at each cortical location: (i) a "best" stimulus orientation, corresponding to the stimulus orientation that elicits a maximal response, and (ii), the magnitude of the response to the best orientation. This mapping has been described as continuous except at a set of singular points (also termed "vortices" [1] or "pinwheels" [2]). Although prior work has shown that vortex pattersn qualitatively similar to the ones observed in visual area 17 of the Macaque cortex can be produced by either band-pass [3] [4] or low-pass [5, 6, 7] filtering of random vector fields, there has been to date little further topological characterization of the structure of cortical vortex patterns. Nevertheless, much theoretical work has been done in other disciplines on mappings analogous to the cortical orientation map. In particular, a recent theorem in the optics literature termed the sign principle [8] states that adjacent vortices on zero crossings of a phase (orientation) Mapping must always alternate in sign. Using digitized samples of recently published optical recording data in monkey striate vortex [9] we show that the cortical orientation data does indeed possess 100% anti-correlation in vortex sign for next-neighbor vortices, as predicted by the sign theorem.This provides strong experimental support for the assumptions of continuity of cortieal vortex maps which underly the sign theorern. Similar analysis predicts a lack of "higher order" vortices in the cortieal orientation map, which is also found to he in agreenment with optical imaging observations. It also follows from this work that cortieal vortices must be created simultaneously in clockwisewise-anti-clockwise pairs. This suggests a possible basis for a modular (hyper-columnar) relationship among pairs of cortieal vortices that originate at the same developmental time. In summary, this work indicates that primate visual cortex orientation column structure is best understood in the context of other "ordered continuous media", (e.g. liquid He^3 , cholesteric liquid crystals, random optical phase maps, to name only a few) in which an order parameter (orientation in this ease) is mapped to a physical space, and in which the topological properties of the mapping determine the observable regularities of the system. We also point out that these methods may well be applied to a variety of other cortical ,ap systemns which admit an "order parameter", i.e. for which each cortical position is assigned a continuous stimulus value.National Institute of Mental Health (5R01MH45969); Office of Naval Research (N00014-95-1-0409