The functional asymmetry of ON and OFF channels in the perception of contrast

Abstract

-To fully understand the relationship between perception and single neural responses, one should take into consideration the early stages of sensory processing. Few studies, however, have directly examined the neural underpinning of visual perception in the lateral geniculate nucleus (LGN), only one synapse away from the retina. In this study we recorded from LGN parvocellular (P) ON-center and OFF-center neurons while monkeys either passively viewed or actively detected a full range of contrasts. We found that OFF neurons were more sensitive in detecting negative contrasts than ON neurons were in detecting positive contrasts. Also, OFF neurons had higher spontaneous activities, higher peak response amplitudes, and were more sustained than ON neurons in their contrast responses. Puzzlingly, OFF neurons failed to show any significant correlations with the monkeys' perceptual choices, despite their greater contrast sensitivities. If, however, choice probabilities were calculated from interspike intervals instead of spike counts (thus taking into account the higher firing rates of OFF neurons), OFF neurons but not ON neurons were significantly correlated with behavioral choices. Taken together, these results demonstrate in awake, behaving animals that: 1) the ON and OFF pathways do not simply mirror each other in their functionality but instead carry qualitatively different types of information, and 2) the responses of ON and OFF neurons can be correlated with perceptual choices even in the absence of physical stimuli and interneuronal correlations. lateral geniculate nucleus; ON-center cell; OFF-center cell; contrast detection; choice probability EARLY PSYCHOPHYSICAL STUDIES indicated that separate channels underlie our perception of brightness (i.e., positive contrasts, or luminance increments) and darkness (i.e., negative contrasts, or luminance decrements), respectively

A stimulus artefact undermines the evidence for independent ON and OFF channels in stereopsis

“…This could enable more dots to be successfully matched up, increasing the number N of disparities which can be averaged on each side of the step-edge and so improving performance. They suggested that the independent processing of black and white dots could be mediated by the separate ON and OFF channels that are well-established early in the visual system (Jiang, Purushothaman, & Casagrande, 2015;Schiller, 2010;Schiller, 1992).…”

Functional Asymmetries between Central and Peripheral Retinal Ganglion Cells in a Diurnal Rodent

“…It has been also reported asymmetries between ON and OFF RGCs population in terms of transient or sustained response. Jiang et al (2015), analyzing retinal data from non-human primates, encountered OFF neurons having higher spontaneous activities, higher peak response amplitudes and with a more sustained temporal response compared to ON neurons. Nevertheless, we only observed asymmetries between central and peripheral RGCs, not particularly associated to ON or OFF populations.…”

“…A recent study in primate retina emphasizes the differences in the electrophysiological response of a single RGC anatomical type (Midget) located in foveal, center and peripheral retina regions (Sinha et al, 2017; Masland, 2017), revealing different functional properties associated to a single RGC type. However, different functional properties for the entire RGC populations remain unknown together with the asymmetries present between ON and OFF cell population at different locations of the visual field (Chichilnisky and Kalmar, 2002; Zaghloul et al, 2003; Liang and Freed, 2010; Jiang et al, 2015; Leonhardt et al, 2016).…”

A normalized contrast-encoding model exhibits bright/dark asymmetries similar to early visual neurons

“…; Jiang et al. ). ON/OFF asymmetries also extend to neuronal spatial receptive fields and temporal properties (Dacey and Petersen ; Chichilnisky and Kalmar ; Pandarinath et al.…”

“…Intuitively, neurons in the ON and OFF pathways might be expected to respond similarly to stimuli of equal and opposite contrast. But in fact, the contrast response functions of ON and OFF neurons have systematic differences (Chichilnisky and Kalmar 2002;Zaghloul et al 2003;Liang and Freed 2010;Kremkow et al 2014;Jiang et al 2015). ON/OFF asymmetries also extend to neuronal spatial receptive fields and temporal properties (Dacey and Petersen 1992;Chichilnisky and Kalmar 2002;Pandarinath et al 2010;Ratliff et al 2010;Jin et al 2011;Nichols et al 2013).…”