Lack of Patchy Horizontal Connectivity in Primary Visual Cortex of a Mammal without Orientation Maps

Abstract

In the cerebral cortex of mammals, horizontal connections link cells up to several millimeters apart. In primary visual cortex (V1) of mammals with orientation maps, horizontal connections ramify in periodic patches across the cortical surface, connecting cells with similar orientation preferences. Rodents have orientation-selective cells but lack orientation maps, raising questions about relationships of horizontal connections to functional maps and receptive field properties. To address these questions, we studied anatomy of horizontal connections and characterized horizontal functional interactions in V1 of the gray squirrel, a highly visual rodent. Long-range intrinsic connections in squirrel V1 extended 1-2 mm but were not patchy or periodic. This result suggests that periodic and patchy connectivity is not a universal organizing principle of cortex, and the existence of patchy and periodic connectivity and functional maps may be linked. In multielectrode and intracellular recordings, we found evidence of unselective local interactions among cells, similar to pinwheel centers of carnivores. These data suggest that, in mammals with and without orientation maps, local connections link near neighbors without regard to orientation selectivity. In single-unit recordings, we found length-summing and end-stopped cells that were similar to those in other mammals. Length-summing cell surrounds were orientation selective, whereas surrounds of end-stopped cells were not. Receptive field response classes are quite similar across mammals, and therefore patchy and columnar connectivity may not be essential for these properties.

Area map of mouse visual cortex

“…10B). This conclusion is consistent with findings that rodent visual cortex lacks a modular organization (Van Hooser et al, 2006) and with observations that the different maps in lateral extrastriate cortex have distinct connections, re- (Fig. 9), and stimulus selectivities (Sanderson et al, 1991;Coogan and Burkhalter, 1993;Burkhalter, 2004, 2005;Gao et al, 2006).…”

Models of cortical networks with long-range patchy projections

“…It provides the baseline to compare with in order to pin down the effect of spatially clustered connectivity patterns. Moreover, at a first glance, this model represents the findings of van Hooser et al (2006), who claim the absence of patchy connections in the primary visual cortex of mammals without orientation maps (see also Random patches below and Section 5).…”

“…In terms of neuroanatomical data, it corresponds to Johnson et al (2000) who state that the PC projections in the piriform cortex of the rat show very little overlap. Later on, we will discuss why the results of van Hooser et al (2006) are probably better represented by this RP than by the NP model.…”

Stereotypical Bouton Clustering of Individual Neurons in Cat Primary Visual Cortex

“…However, axonal and dendritic trees are structures of considerable spatial complexity (Gilbert and Wiesel, 1981;Binzegger et al, 2004). In the cat, tree shrew, and monkey cortex, but not in rodents (Hooser et al, 2006), the axons of many spiny neurons form long laterally directed collaterals that branch to form clusters of terminal boutons Lund, 1982, 1983;Gilbert and Wiesel, 1983;Martin and Whitteridge, 1984). These patchy projections were first seen for the ocular dominance system in area 17 of the primate, where the thalamic afferents not only form the retinotopic map on the cortex but also segregate anatomically into left and right eye dominated clusters or "columns" (Hubel and Wiesel, 1969).…”