Temporal Asymmetry in Dark-Bright Processing Initiates Propagating Activity across Primary Visual Cortex.

Differences between visual pathways representing darks and lights have been shown to affect spatial resolution and detection timing. Both psychophysical and physiological studies suggest an underlying retinal origin with amplification in primary visual cortex (V1). Here we show that temporal asymmetries in the processing of darks and lights create motion in terms of propagating activity across V1. Exploiting the high spatiotemporal resolution of voltage-sensitive dye imaging, we captured population responses to abrupt local changes of luminance in cat V1. For stimulation we used two neighboring small squares presented on either bright or dark backgrounds. When a single square changed from dark to bright or vice versa, we found coherent population activity emerging at the respective retinal input locations. However, faster rising and decay times were obtained for the bright to dark than the dark to bright changes. When the two squares changed luminance simultaneously in opposite polarities, we detected a propagating wave front of activity that originated at the cortical location representing the darkened square and rapidly expanded toward the region representing the brightened location. Thus, simultaneous input led to sequential activation across cortical retinotopy. Importantly, this effect was independent of the squares' contrast with the background. We suggest imbalance in dark-bright processing as a driving force in the generation of wave-like activity. Such propagation may convey motion signals and influence perception of shape whenever abrupt shifts in visual objects or gaze cause counterchange of luminance at high-contrast borders. SIGNIFICANCE STATEMENT: An elementary process in vision is the detection of darks and lights through the retina via ON and OFF channels. Psychophysical and physiological studies suggest that differences between these channels affect spatial resolution and detection thresholds. Here we show that temporal asymmetries in the processing of darks and lights create motion signals across visual cortex. Using two neighboring squares, which simultaneously counterchanged luminance, we discovered propagating activity that was strictly drawn out from cortical regions representing the darkened location. Thus, a synchronous stimulus event translated into sequential wave-like brain activation. Such propagation may convey motion signals accessible in higher brain areas, whenever abrupt shifts in visual objects or gaze cause counterchange of luminance at high-contrast borders.

Primary visual cortex represents the difference between past and present.

The visual system is confronted with rapidly changing stimuli in everyday life. It is not well understood how information in such a stream of input is updated within the brain. We performed voltage-sensitive dye imaging across the primary visual cortex (V1) to capture responses to sequences of natural scene contours. We presented vertically and horizontally filtered natural images, and their superpositions, at 10 or 33 Hz. At low frequency, the encoding was found to represent not the currently presented images, but differences in orientation between consecutive images. This was in sharp contrast to more rapid sequences for which we found an ongoing representation of current input, consistent with earlier studies. Our finding that for slower image sequences, V1 does no longer report actual features but represents their relative difference in time counteracts the view that the first cortical processing stage must always transfer complete information. Instead, we show its capacities for change detection with a new emphasis on the role of automatic computation evolving in the 100-ms range, inevitably affecting information transmission further downstream.

Independent encoding of grating motion across stationary feature maps in primary visual cortex visualized with voltage-sensitive dye imaging.

In early visual cortex different stimulus parameters are represented in overlaid feature maps. Such functioning was extensively explored by the use of drifting gratings characterized by orientation, spatial-temporal frequency, and direction of motion. However surprisingly, the direct cortical visuotopic drift of the gratings' stripy pattern has never been detected simultaneously to these stationary feature maps. It therefore remains to be demonstrated how physical signals of grating motion across the cortex are represented independently of other parametric maps and thus, how multi-dimensional input is processed independently to enable effective read-out further downstream. Taking advantage of the high spatial and temporal resolution of voltage-sensitive dye imaging, we here show the real-time encoding of position and orientation. By decomposing the cortical responses to drifting gratings we visualize the typical emergence of stationary orientation maps in which specific domains exhibited highest amplitudes. Simultaneously to these patchy maps, we demonstrate coherently propagating waves of activity that precisely matched the actual movement of the gratings in space and time, most dominantly for spatial frequencies lower than the preferred range. Thus, the primary visual cortex multiplexes information about retinotopic motion by additional temporal modulation of stationary orientation signals. These signals may be used to variably extract coarse-grained object motion and form information at higher visual processing stages.