Brightness in human rod vision depends on slow neural adaptation to quantum statistics of light

Abstract

In human rod-mediated vision, threshold for small, brief flashes rises in proportion to the square root of adapting luminance at all but the lowest and highest adapting intensities. A classical signal detection theory from Rose (1942, 1948) and de Vries (1943) attributed this rise to the perceptual masking of weak flashes by Poisson fluctuations in photon absorptions from the adapting field. However, previous work by Brown and Rudd (1998) demonstrated that the square-root law also holds for suprathreshold brightness judgments, a finding that supports an alternative explanation of the square-root sensitivity changes as a consequence of physiological adaptation (i.e., neural gain control). Here, we employ a dichoptic matching technique to investigate the properties of this brightness gain control. We show that the brightness gain control: 1) affects the brightness of high-intensity suprathreshold flashes for which assumptions of the de Vries-Rose theory are strongly violated; 2) exhibits a long time course of 100-200 s; and 3) is subject to modulation by temporal contrast noise when the mean adapting luminance is held constant. These findings are consistent with the hypothesis that the square-root law results from a slow neural adaptation to statistical noise in the rod pool. We suggest that such adaptation may function to reduce the probability of spurious ganglion cell spiking activity due to photon fluctuation noise as the ambient illumination level is increased.

The Influence of Physical Illumination on Lightness Perception in Simultaneous Contrast Displays

“…Such finding was neither in line with Jameson and Hurvich’s results, nor with illumination-independent constancy findings. (b) We found that, in general, both targets in SLC configurations (except for the configuration reduced ) appeared darker in the low illumination range, and the magnitude of SLC was reduced ( Rudd & Rieke, 2016 ), though magnitudes were significantly different (over 1 Munsell step) only compared with the magnitudes of the double Gelb lighting condition for configurations enhanced and ramps . (c) However, with regard to configurations enhanced and ramps , the target on the white background did not get darker but remained virtually constant in lightness across the normal illumination range, as predicted by the anchoring theory ( Economou et al., 2007 ).…”

“…With regard to the second point, the low range showed a general darkening of SLC targets in all configurations. This finding implies that the Weber’s law—and therefore constancy—may not hold up under scotopic conditions (for a thorough discussion on the issue, see Rudd & Rieke, 2016 ). However, we cannot ensure that the spectral sensitivity of ambient illumination condition was within a scotopic luminous efficiency range in the illumination conditions that fall within the low range in Experiments 1 and 2, given that the methods for calculating lighting levels in the existing literature actually refer only to a “luminous quantity” that falls on a surface ( Saunders, Jarvis, & Wathes, 2008 ).…”

“…One might be tempted to consider the low range as taking place within scotopic illumination conditions. This would be convenient, as Rudd and Rieke (2016) offered an account on lightness constancy failures in scotopic vision based on findings derived from experiments aimed at studying the properties of the brightness gain control function. However, we believe that their account might apply to the darkest Gelb illumination condition (9 f/stop).…”

“…Nevertheless, the isolation hypothesis is not necessarily confuted by the findings of Experiment 2, given that at the lowest Gelb intensities we might have entered or bordered the scotopic luminous efficiency range, an illumination condition in which only rods are active ( Schubert, 2006 ). According to Rudd and Rieke (2016) , under such viewing conditions, the Weber’s law does not hold, and this may account for the general darkening of the targets. This point is further considered in the General Discussion section.…”

Impact of light-adaptive mechanisms on mammalian retinal visual encoding at high light levels

“…Our demonstration that the spatiotemporal receptive field of alpha-type ganglion cells adapts in accordance with reported changes in SNR across light levels (Borghuis et al 2009) raises the question of how this adaptation is achieved at the synaptic and circuit level. A recent psychophysical study in humans reported noise-modulated gain control within the scotopic rod pathway that functions over a time course on the order of 100 s (Rudd and Rieke 2016). Other recent work showed that under fixed stimulus conditions, such as a particular light-adapted state, the response of some OFFtype ganglion cells is optimized for SNR when the strength of excitation and inhibition onto the ganglion cell scale with stimulus strength according to exponential functions with op-posite sign, driven by the same input signal (Homann and Freed 2017).…”