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.

Space-Specific Deficits in Visual Orientation Discrimination Caused by Lesions in the Midbrain Stimulus Selection Network

“…Neurophysiological studies in the Wulst have shown that the retinogeniculate pathway conveys information that is used to construct neurons that are tuned for the orientation of local contours, both in birds with eyes oriented laterally (pigeons, chickens and finches [7–9]) or frontally (owls [6, 10]). Also during this time, the OT has been shown to be the hub of a sophisticated midbrain network that selects and transmits the highest priority visual information for further analysis in the forebrain [2, 21].…”

Catching the voltage gradient—asymmetric boost of cortical spread generates motion signals across visual cortex: a brief review with special thanks to Amiram Grinvald

“…103 Using VSDI, we showed predictive coding in V1 in a strict sense, signifying differences in feature representation (i.e., orientation) of past and present inputs. 109 We also pioneered the use of VSDI in pigeons 110 and showed that these highly visual animals have no orientation maps in the assumed homolog of mammalian V1. Instead, we demonstrated overrepresentation of vertical orientation, possibly as a result of adaptation to biased input statistics.…”

Cortico-cortical Communication Dynamics

“…Part of the explanation might be that the dye signal in vivo reflects synaptic activity at the mesoscopic scale, whereas the action potential recordings capture the activity of single neurons (Lippert et al, 2007;Eriksson et al, 2008). Nevertheless, in several studies one can follow how net increases in the synaptic activity propagate over the cortical areas when the cortex is perturbed by a sensory transient (Senseman, 1996;Prechtl et al, 1997;Senseman and Robbins, 2002;Slovin et al, 2002;Grinvald and Hildseheim, 2004;Roland et al, 2006;Ferezou et al, 2007;Lippert et al, 2007;Xu et al, 2007;Ahmed et al, 2008;Han et al, 2008;Takagaki et al, 2008;Yoshida et al, 2008;Harvey et al, 2009;Ayzenshtat et al, 2010;Meirovithz et al, 2010;Ng et al, 2010;Polack and Contreras, 2012;Harvey and Roland, 2013). This synaptic dynamics may show some order in the feed-forward propagation of net-excitation for example between V1 and V2 in monkeys, rats and turtles, between the barrel field and the motor cortex in the mouse, and between visual areas 17, 18 and 19, 21 in the ferret.…”

“…Some of these studies contain observations of a reverse order of synaptic propagation, that is, from higher areas towards the primary sensory areas, some 40-50 ms later, i.e., 80-100 ms after the stimulus onset Lippert et al, 2007;Xu et al, 2007;Ahmed et al, 2008;Takagaki et al, 2008;Yoshida et al, 2008;Harvey et al, 2009;Ayzenshtat et al, 2010;Ng et al, 2010;Lim et al, 2012; see also Zheng and Yao, 2012;Harvey and Roland, 2013). This mode of propagation has been named feedback.…”