Neuronal nonlinearity explains greater visual spatial resolution for darks than lights

Abstract

Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli, but the neuronal mechanisms for this perceptual asymmetry remain unknown. Here we demonstrate that the asymmetry is caused by a neuronal nonlinearity in the early visual pathway. We show that neurons driven by darks (OFF neurons) increase their responses roughly linearly with luminance decrements, independent of the background luminance. However, neurons driven by lights (ON neurons) saturate their responses with small increases in luminance and need bright backgrounds to approach the linearity of OFF neurons. We show that, as a consequence of this difference in linearity, receptive fields are larger in ON than OFF thalamic neurons, and cortical neurons are more strongly driven by darks than lights at low spatial frequencies. This ON/OFF asymmetry in linearity could be demonstrated in the visual cortex of cats, monkeys, and humans and in the cat visual thalamus. Furthermore, in the cat visual thalamus, we show that the neuronal nonlinearity is present at the ON receptive field center of ONcenter neurons and ON receptive field surround of OFF-center neurons, suggesting an origin at the level of the photoreceptor. These results demonstrate a fundamental difference in visual processing between ON and OFF channels and reveal a competitive advantage for OFF neurons over ON neurons at low spatial frequencies, which could be important during cortical development when retinal images are blurred by immature optics in infant eyes.neuronal coding | lateral geniculate nucleus | area V1 | irradiation illusion | LFP L ight and dark stimuli are separately processed by ON and OFF channels in the retina and visual thalamus. Surprisingly, although most textbooks assume that ON and OFF visual responses are balanced throughout the visual system, recent studies have identified a pronounced overrepresentation of the OFF visual responses in primary visual cortex (area V1) (1-3). This recent discovery resonates with pioneering studies by Galilei (4) and von Helmholtz (5) who noticed that visual spatial resolution was higher for dark than light stimuli. Galilei (4) related the difference in resolution to the observation that a light patch on a dark background appears larger than the same sized dark patch on a light background, an illusion that von Helmholtz (5) named the "irradiation illusion." Although this illusion has been studied in the past (6, 7), its underlying neuronal mechanisms remain unknown. It has been suggested that the perceived size differences could be caused by the light scatter in the optics of the eye followed by a neuronal nonlinearity (6, 7), but there are no neuronal measurements of a nonlinearity that fits the explanation. Previous studies revealed differences in response linearity between ON and OFF retinal ganglion cells (8, 9) and horizontal cells (10). However, a main conclusion from these studies was that ON retinal ganglion cells were roughly linear and less rectified than OFF retinal gangl...

A Contrast and Surface Code Explains Complex Responses to Black and White Stimuli in V1

“…Recent accumulated evidence indicates that neurons in V1 are more sensitive to black than to white stimuli (Jin et al, 2008;Yeh et al, 2009;Xing et al, 2010;Kremkow et al, 2014). Our data support these findings and further show the spatial characteristics of the black/white differences: a strong difference at the squares' center and a weaker difference at the edges.…”

“…More recent neurophysiological studies of single-cell activity in nonhuman primates (Yeh et al, 2009;Xing et al, 2010) found that layer 2/3 neurons responded better to small, localized black spots than to white spots, and also that neurons preferring black outnumbered neurons preferring white stimuli. Others also have observed larger black responses in V1 (Jin et al, 2008;Kremkow et al, 2014). The physiological data on blackwhite preferences are consistent with data from human perceptual experiments (Chubb and Nam, 2000;Chubb et al, 2004).…”

“…In a recent study, Kremkow et al (2014) showed ON/OFF asymmetry in the LGN and V1, which was accounted for by nonlinear processing that was qualitatively different for the two pathways. Our cortical data did not exhibit a clear difference in nonlinearity for all regions ( Fig.…”

“…Previous accounts of the balance between contrast-responsive and surface-responsive neurons in macaque V1 reported that a minority, between 20 and 40%, of neurons respond to uniform surfaces (Peng and Van Essen, 2005;Huang and Paradiso, 2008;Dai and Wang, 2012). Electrophysiological studies of black versus white asymmetry report ratios of ϳ2-3 (Yeh et al, 2009;Xing et al, 2010) and 1.9 -2.1 (Kremkow et al, 2014). The correspondence between our model's parameters and known attributes of V1 from the literature is an indication of the validity of the proposed model.…”

Refractory Sampling Links Efficiency and Costs of Sensory Encoding to Stimulus Statistics

“…So, under selection pressures, adaptation to prevailing conditions (Darwin, 1859) characteristically improves efficiency and performance of living systems (see also de Polavieja, 2004;Pérez-Escudero et al, 2009). Recent studies indicate that natural light environment is asymmetrical, containing more dark than light patches (Ratliff et al, 2010) and that this affects how retinae and brains of animals have adapted to represent the world neurally (Ratliff et al, 2010; Kremkow et al, 2014). In this work, we presented evidence that information sampling in fly photoreceptors may already use this asymmetry to accentuate responses to naturalistic light stimuli, improving vision and likely the flies' fitness.…”