The Shape of Dendritic Arbors in Different Functional Domains of the Cortical Orientation Map

Abstract

The neocortex is organized into macroscopic functional maps. However, at the microscopic scale, the functional preference and degree of feature selectivity between neighboring neurons can vary considerably. In the primary visual cortex, adjacent neurons in iso-orientation domains share the same orientation preference, whereas neighboring neurons near pinwheel centers are tuned to different stimulus orientations. Moreover, several studies have found greater orientation selectivity in iso-orientation domains than in pinwheel centers. These differences suggest that neurons sample local inputs in a spatially homogenous fashion and independently of the location of their soma on the orientation map. Here we determine whether dendritic geometry is affected by neuronal position on the orientation map. We labeled individual layer 2/3 pyramidal neurons with fluorescent dyes in specific domains of the orientation map in cat primary visual cortex and imaged their dendritic trees in vivo by two-photon microscopy. We found that the circularity and uniformity of dendritic trees is independent of somatic position on the orientation map. Moreover, the dendrites of neurons located close to pinwheel centers extend across all orientation domains in an unbiased fashion. Thus, unbiased dendritic trees appear to provide an anatomical substrate for the systematic variations in feature selectivity across the orientation map.

Differences in orientation tuning between pinwheel and domain neurons in primary visual cortex depend on contrast and size

“…The discovery of this unique organization enabled comparisons between homogeneous (domains) and heterogeneous (pinwheel) regions with respect to the orientation preference of local populations of neurons. [19][20][21][22][23][24][25][26][27] Using this technique, our work and the work of others have shown that pinwheels in the primary visual cortex correlate to poorer orientation selectivity of their component neurons as compared to domain regions. [28][29][30][31] This lower selectivity can occur specifically for optimally sized classical receptive field (CRF) stimuli, where the relatively small stimulus size elicits the maximum response, and where the driving mechanisms are largely feedforward and local cortical circuits.…”

Functional implications of orientation maps in primary visual cortex

“…Using two-photon imaging, Levy et al 44. found no relationship between the geometry of the dendritic arbour and the local homogeneity in the orientation map, suggesting that all layer 2/3 neurons integrate inputs similarly from all their neighbours.…”

Contrast and response gain control depend on cortical map architecture

“…This anatomical organization has significant implications for cortical development and imposes restrictions on the connectivity of cells within the map (Alexander & Leeuwen, ), partly because the dendritic fields of the neurons within the cortex tend to be near‐circular wherever they are positioned in the map (Martin & Whitteridge, ; Levy et al ., ). Therefore, local connections at pinwheel centres occur between neurons with many orientation preferences, whereas connections in iso‐orientation zones are between neurons with similar orientation preference (primate: Malach et al ., ; cat: Levy et al ., ).…”

“…Neurons with selectivity for similar stimulus features are clustered together (orientation: Hubel & Wiesel, , ; ocular dominance: Blasdel & Salama, ; Ts'o et al ., ; Kara & Boyd, ; binocular disparity: Kara & Boyd, ; spatial frequency: Hübener et al ., ; Kim et al ., ; Issa et al ., ; Sirovich & Uglesich, ; Yu et al ., ; Nauhaus et al ., ; surround suppression: Vanni & Casanova, ). This anatomical organization has significant implications for cortical development and imposes restrictions on the connectivity of cells within the map (Alexander & Leeuwen, ), partly because the dendritic fields of the neurons within the cortex tend to be near‐circular wherever they are positioned in the map (Martin & Whitteridge, ; Levy et al ., ). Therefore, local connections at pinwheel centres occur between neurons with many orientation preferences, whereas connections in iso‐orientation zones are between neurons with similar orientation preference (primate: Malach et al ., ; cat: Levy et al ., ).…”

“…Cells in pinwheel centres have broader orientation tuning, as measured at the membrane potential level (Schummers et al ., ), but not at the spiking level (Maldonado et al ., ; Nauhaus et al ., ). The local connections to cells within pinwheel centres are more likely to come from cells with a range of preferred orientations, whereas in iso‐orientation zones local connections are more likely to come from cells with similar orientation tuning (Levy et al ., ).…”