Dominant Vertical Orientation Processing without Clustered Maps: Early Visual Brain Dynamics Imaged with Voltage-Sensitive Dye in the Pigeon Visual Wulst

Abstract

The pigeon is a widely established behavioral model of visual cognition, but the processes along its most basic visual pathways remain mostly unexplored. Here, we report the neuronal population dynamics of the visual Wulst, an assumed homolog of the mammalian striate cortex, captured for the first time with voltage-sensitive dye imaging. Responses to drifting gratings were characterized by focal emergence of activity that spread extensively across the entire Wulst, followed by rapid adaptation that was most effective in the surround. Using additional electrophysiological recordings, we found cells that prefer a variety of orientations. However, analysis of the imaged spatiotemporal activation patterns revealed no clustered orientation map-like arrangements as typically found in the primary visual cortices of many mammalian species. Instead, the vertical orientation was overrepresented, both in terms of the imaged population signal, as well as the number of neurons preferring the vertical orientation. Such enhanced selectivity for the vertical orientation may result from horizontal motion vectors that trigger adaptation to the extensive flow field input during natural behavior. Our findings suggest that, although the avian visual Wulst is homologous to the primary visual cortex in terms of its gross anatomical connectivity and topology, its detailed operation and internal organization is still shaped according to specific input characteristics.