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

Abstract

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.

Context-dependent lightness affects perceived contrast

“…However perceived contrast of decremental gratings were not systematically studied previously under conditions similar to those reported here. Processing differences between positive and negative local contrast has been reported in literature both by behavioral and neuronal studies (e.g., Chubb & Nam, 2000;Rekauzke et al, 2016;Rudd & Zemach, 2004Sato et al, 2016;Whittle, 1986;Zaghloul et al, 2003). The light-dark asymmetry is also incorporated in some models of brightness (e.g., Rudd, 2013Rudd, , 2014.…”

“…4). Using rectified gratings allowed us to study positive and negative contrast patterns independently, which was critical because both behavioral and neural evidence in previous studies suggest fundamental differences between processing of incremental and decremental luminance patterns (e.g., Blackwell, 1946;Chubb & Nam, 2000;Economou, Zdravkovic, & Gilchrist, 2007;Kremkow, Jin, Wang, & Alonso, 2016;Patel & Jones, 1968;Rekauzke et al, 2016;Rudd & Zemach, 2004Sato, Motoyoshi, & Sato, 2016;Whittle, 1986;Zaghloul, Boahen, & Demb, 2003). Previous studies in literature have found interactions between spatial frequency and mean luminance in contrast perception using simple gratings (Chubb, Sperling, & Solomon, 1989;Georgeson & Sullivan, 1975;Peli et al, 1996;Robilotto & Zaidi, 2004;Van & Bouman, 1967).…”

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

“…[118][119][120] Here, two examples in the visual domain were presented, where propagation of cortical activity emerges from local spacetime imbalances in the computation of external input. 20,21 The crucial factor for both instances is that local input creates cortical spread, which builds up a gradient of activity-from subthreshold to suprathreshold levels. The initial temporal advance in the generation of precuing activity enables subsequent input to boost asymmetric propagation of suprathreshold activity in V1.…”

“…In support of this idea, we recently showedusing another paradigm that creates apparent motion perception in humans-how asymmetrically propagating activity resembles the perceived direction of motion. 21 Once again, the high spatiotemporal resolution of VSDI enabled us to track activity Histological section of cortical tissue after staining with cytochrome oxidase that visualizes the regular mosaic pattern of oxidase blobs in V1 (Macaque monkey). The small square in the center of the image approximates the region that is activated by feedforward thalamic input using a visual stimulus as small as 0.5 deg × 0.25 deg in size.…”

“…[66][67][68][69][70] Thus, motion streaks may be analyzed unconsciously and separately over time [71][72][73][74] to contribute to further analysis such as form-from-motion at higher processing stages. 20,21,62,69,70,[75][76][77][78][79][80] Interactions mediated by propagating waves of cortical population activity across V1 have been demonstrated for a variety of mammalian species (for example, see Refs. 20 and 81-91).…”