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Optimum Spatiotemporal Receptive Fields for Vision in Dim Light

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Optimum Spatiotemporal Receptive Fields for Vision in Dim Light Journal of Vision (2009) 9(4):18, 1–16 http://journalofvision.org/9/4/18/ 1 Optimum spatiotemporal receptive fields for vision in dim light Department of Neuroscience, Karolinska Institute, Stockholm, Sweden,& Department of Cell and Organism Biology, Lund University, Andreas Klaus Lund, Sweden Department of Cell and Organism Biology, Lund University, Eric J. Warrant Lund, Sweden Many nocturnal insects depend on vision for daily life and have evolved different strategies to improve their visual capabilities in dim light. Neural summation of visual signals is one strategy to improve visual performance, and this is likely to be especially important for insects with apposition compound eyes. Here we develop a model to determine the optimum spatiotemporal sampling of natural scenes at gradually decreasing light levels. Image anisotropy has a strong influence on the receptive field properties predicted to be optimal at low light intensities. Spatial summation between visual channels is predicted to extend more strongly in the direction with higher correlations between the input signals. Increased spatiotemporal summation increases signal-to-noise ratio at low frequencies but sacrifices signal-to-noise ratio at higher frequencies. These results, while obtained from a model of the insect visual system, are likely to apply to visual systems in general. Keywords: neural summation, apposition compound eye, receptive field, anisotropy, signal-to-noise ratio, optimization Citation: Klaus, A., & Warrant, E. J. (2009). Optimum spatiotemporal receptive fields for vision in dim light. Journal of Vision, 9(4):18, 1–16, http://journalofvision.org/9/4/18/, doi:10.1167/9.4.18. Nilsson, 1989; Warrant, 2004). A general strategy to Introduction increase light capture is to simply increase eye size (Jander & Jander, 2002; Land & Nilsson, 2002). This, Vision is an important sense for most species within the however, is constrained by the metabolic costs of neural animal kingdom and even in the dimmest habitats animals information processing (Laughlin, de Ruyter van Steveninck, have functional eyes (Warrant, 2004). A nocturnal life- & Anderson, 1998; Niven, Andersson, & Laughlin, 2007), style has several advantages, such as reduced predation and by locomotory costs (especially for flying insects), pressure and access to underexploited sources of food introduced by the additional weight of the eyes. (Roubik, 1989; Warrant, Porombka, & Kirchner, 1996; In addition to optical improvements, visual sensitivity Wcislo et al., 2004). However, nocturnal life also has a can also be increased by neural adaptations. Adjacent crucial disadvantage: the scarcity of light. At night, light points in natural images are correlated, and this correla- intensities can be up to 9 orders of magnitude lower than tion falls exponentially as the distance between the points during the day at the same location and this scarcity of increases (Srinivasan, Laughlin, & Dubs, 1982), a fact that light can make vision unreliable: visual signals in dim has been further studied by analyzing the power spectra of light are contaminated by visual “noise”. Part of this noise natural scenes (van der Schaaf & van Hateren, 1996). The arises from the stochastic nature of photon arrival and spectral power in terrestrial images falls with increasing 2 absorption: each sample of absorbed photons (or signal) spatial frequency fs as 1/fs (Dong & Atick, 1995; Field, has a certain degree of uncertainty (or noise) associated 1987; Simoncelli & Olshausen, 2001; van der Schaaf & with it. The relative magnitude of this uncertainty is van Hateren, 1996). Due to correlation within natural greater at lower rates of photon absorption, and these images, neighboring visual channels share some informa- quantum fluctuations set an upper limit to the visual tion, and thus a proportion of the signal generated in one signal-to-noise ratio (de Vries, 1943; Rose, 1942). The channel can be predicted from the signals generated in dimmer the light level, the lower the signal-to-noise ratio neighboring channels (Srinivasan et al., 1982; Tsukamoto, (Land, 1981; Snyder, 1979), and a visual system straining Smith, & Sterling, 1990; van Hateren, 1992c). In bright to see at night should therefore capture as much light as light this “predictive coding” leads to visual sampling possible. This can be achieved optically by enlarging the involving lateral inhibition between adjacent channels receptive fields of the photoreceptors and/or by widening (band-pass filtering), whereas in dim light sampling the pupil of the eye (Kirschfeld, 1974; Land, 1981; involves spatial summation of signals from groups of doi: 10.1167/9.4.18 Received November 3, 2008; published April 22, 2009 ISSN 1534-7362 * ARVO Downloaded from jov.arvojournals.org on 04/06/2019 Journal of Vision (2009) 9(4):18, 1–16 Klaus & Warrant 2 neighboring channels (low-pass filtering). As shown the apposition compound eye (Figure 1B), a design in theoretically, a strategy of neural summation of light in which single photoreceptors receive light only from the space and time can enable an eye to improve visual single corneal facet lens residing in the same ommati- reliability in dim light (Tsukamoto et al., 1990; van dium. Not surprisingly, apposition eyes are typical of Hateren, 1992c; Warrant, 1999). Neural summation will, diurnal insects active in bright sunlight, such as bees, flies, however, cause a decrease in spatial and temporal butterflies, and dragonflies. Interestingly, despite their resolution (Warrant, 1999). disadvantages for vision in dim light, some nocturnal Despite its difficulties, many nocturnal animalsV insects have apposition compound eyes. In tropical rain- including insectsVrely on vision for the tasks of daily forests, for instance, the competition for resources and the life (Warrant, 2007, 2008a). Insects have compound eyes, threat of predation are fierce, and many species of bees an eye type constructed from an assembly of repeated and waspsVall with apposition eyesVhave evolved a optical units, the “ommatidia” (Figure 1A). Nocturnal nocturnal lifestyle, an evolutionary transition that is insects, including most moths and many beetles, typically probably relatively recent (Wcislo et al., 2004). Animals have refracting superposition compound eyes, a design with apposition eyes have evolved a number of adapta- that allows single photoreceptors in the retina to receive tions that improve sensitivity in dim light (Barlow, focussed light from hundreds (and in some extreme cases, Kaplan, Renninger, & Saito, 1987;Warrant,2007, thousands) of corneal facet lenses (Figure 1C). This 2008b) and that allow visually guided behavior at lowest design represents a vast improvement in sensitivity over light intensities (Barlow & Powers, 2003; Warrant et al., 2004). For example, the apposition eyes of the nocturnal sweat bee, Megalopta genalis, possess larger corneal facet lenses and wider rhabdoms than those of closely related diurnal bees, and thus enjoy an increased optical sensi- tivity (Greiner, Ribi, & Warrant, 2004). Further improve- ments in visual sensitivity are likely to come from enhanced visual gain in the photoreceptors (Barlow, Bolanowski, & Brachman, 1977; Barlow et al., 1987; Frederiksen, Wcislo, & Warrant, 2008) and from a strategy of visual summation in space and time (Theobald, Greiner, Wcislo, & Warrant, 2006; Warrant et al., 2004). Morphological, electrophysiological, and theoretical evi- dences (Warrant, 2008b) suggest that widely arborizing second-order cells in the lamina (the LMC cells) might mediate a spatial summation of visual signals generated in the retina (Greiner, Ribi, & Warrant, 2005; Greiner, Ribi, Wcislo, & Warrant, 2004). Figure 1. Compound eyes. (A) A schematic longitudinal section Thus, when a diurnal insect with apposition eyesVlike (and an inset of a transverse section) through a generalized the ancestor of the nocturnal bee MegaloptaVbegan to Hymenopteran ommatidium (from an apposition eye, see B), evolve a nocturnal lifestyle, the optical and neural showing the corneal lens (c), the crystalline cone (cc), the primary structures of the eye altered according to natural selection pigment cells (pc), the secondary pigment cells (sc), the rhabdom (Frederiksen & Warrant, 2008). As the diurnal ancestor (rh), the retinula cells (rc), the basal pigment cells (bp), and the conquered dimmer and dimmer niches, its eyes evolved basement membrane (bm). The upper half of the ommatidium greater sensitivity: widening rhabdoms increased the shows screening pigment granules in the dark-adapted state, while visual fields of the photoreceptors, and the dendritic trees the lower half shows them in the light-adapted state. Redrawn from of the LMC cells became more extensive, possibly in Stavenga and Kuiper (1977), with permission. (B) A focal order to mediate spatial summation. How should these apposition compound eye. Light reaches the photoreceptors optical and neural changes evolve in order to continuously exclusively from the small corneal lens (co) located directly provide optimal visual performance during the evolution above, within the same ommatidium. This eye design is typical of a nocturnal lifestyle? of day-active insects. cc = crystalline cone. (C) A refracting The aim of this investigation is to model how an array superposition compound eye. A large number of corneal facets, of visual channels samples natural grayscale scenes at and bullet-shaped crystalline cones of circular cross-section different light intensities and image velocities. How, for
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