RAPID COMMUNICATION Ocular Dominance Peaks at Pinwheel Center Singularities of the Orientation Map in Cat Visual Cortex

Crair, Michael C., Edward S. Ruthazer, Deda C. Gillespie, and findings but also yields some insight into development and Michael P. Stryker. Ocular dominance peaks at pinwheel center possible function. singularities of the orientation map in cat visual cortex. J. Neurophysiol. 77: 3381–3385, 1997. In the primary visual cortex of monM E T H O D S key and cat, ocular dominance and orientation are represented continuously and simultaneously, so that most neighboring neurons reOptical imaging spond optimally to visual stimulation of the same eye and Optical intrinsic signal responses were measured using standard orientation. Maps of stimulus orientation are punctuated by singularitechniques (for review, see Bonhoeffer and Grinvald 1996). ties referred to as ‘‘pinwheel centers,’’ around which all orientations Briefly, reflectance of primary cat visual cortex (AP 02.0 to 2.0, are represented. Given that the orientation map is mostly continuous, close to the V1/V2 border, illuminated with 610-nm light) followorientation singularities are a mathematical necessity unless the map ing monocular presentation of moving high-contrast square wave consists of perfectly parallel rows, and there is no evidence that the gratings (0.1–0.2 cycles/deg, 1 cycle/s, 8 orientations separated singularities play a role in normal function or development. We by 22.5 deg in pseudorandom order) was captured at 192 1 144 report here that in cats there is a strong tendency for peaks of pixel resolution through a matching 610-nm filter by a cooled slow ocular dominance to lie on the pinwheel center singularities of the scan CCD Camera (Princeton Instruments, NJ). Images were highorientation map. This relationship predicts but is not predicted by pass filtered (1.2-mm kernel) and smoothed (50 mm kernel) when the tendencies, previously reported, for pinwheels to lie near the necessary. Cortical responses to the presentation of different stimucenter lines of ocular dominance bands and for iso-orientation bands lus orientations were combined and summarized using a single to cross ocular dominance boundaries at right angles. The coincipseudocolor representation referred to as an angle map. Ocular dence of ocular dominance peaks with orientation singularities is dominance (OD) ratio maps were computed by adding up the likely to reflect a strong underlying functional link between the two responses to all stimuli presented to the left eye and dividing by visual cortical maps. the sum of the responses to stimuli presented to the right eye. Orientation images used in this paper were responses to a particular oriented stimulus divided by the average response to all orientaI N T R O D U C T I O N tions through either eye (sometimes referred to as a ‘‘cocktail blank’’ normalization). Hubel and Wiesel described maps for both orientation and eye preference in visual cortex and proposed a unified model Analysis in which the representation of ocular dominance ran orthogoThe center lines of ocular dominance bands were computed from nal to bands of like orientation preference (Hubel and Wiesel OD ratio maps using the medial axis transform (IDL, Research 1974), assuring representation of all orientations through Systems). To determine unambiguously the positions of the peaks both eyes. While later imaging studies revised this model in of the functional ocular dominance domains, the centroids of redetail (Blasdel and Salama 1986; Grinvald et al. 1986; Hubel gions within the full-width, half-maximum response contour of the et al. 1978), revealing singularities of unknown function band-pass filtered OD ratio maps were computed. The positions of pinwheel singularities were defined as the points where the integral in the orientation map around which all orientations were of the orientation differences around a pixel was {1807. Angle represented (Blasdel 1992; Bonhoeffer and Grinvald 1993; maps were smoothed when necessary using a 3-bin Lee filter (IDL) Rojer and Schwartz 1990), one of its features, the tendency to prevent identification of spurious pinwheels. for iso-orientation lines (along which orientation preference does not change) to cross the boundaries of ocular domiR E S U L T S nance domains at right angles, was confirmed in monkey (Bartfeld and Grinvald 1992; Obermayer and Blasdel 1993). Maps of orientation and ocular dominance from seven The same imaging studies also revealed a tendency for pincats (P26-P55) with normal visual experience were obtained wheel center singularities of the orientation map to lie along by imaging intrinsic optical signals (Bonhoeffer and Grinthe center lines of ocular dominance bands. Similar results vald 1993, 1996). Figure 1 shows a typical activity pattern have been reported in cat (Hubener et al. 1995). in a cat. Response to oriented stimuli is patchy and heterogeWe sought to determine whether a closer relationship neous, with different areas of cortex responding to different might exist between the representations of eye preference stimulus orientations. In total, this response tiles the cortex and stimulus orientation than those previously reported. We into a single orientation map, which consists of regions of smooth change in orientation preference and singularities found such a relationship, which not only predicts the earlier