Bees encode behaviorally significant spectral relationships in complex scenes to resolve stimulus ambiguity

Lotto, R. Beau; Wicklein, Martina

doi:10.1073/pnas.0503773102

Cited by 18 publications

(16 citation statements)

References 18 publications

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“…However, this limitation can, to a certain degree, be overcome in simpler systems (natural or synthetic) by raising and/or evolving them in highly controlled visual ecologies. This has been successfully achieved with experiments of bumblebees [35] and artificial-life systems [36]. Here we directly explored the empirical basis of human brightness and lightness perception by taking advantage of the fact that the visual system is differentially sensitive to wavelength.…”

Section: Discussionmentioning

confidence: 99%

The Brightness of Colour

Corney¹,

Haynes

Rees

et al. 2009

PLoS ONE

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BackgroundThe perception of brightness depends on spatial context: the same stimulus can appear light or dark depending on what surrounds it. A less well-known but equally important contextual phenomenon is that the colour of a stimulus can also alter its brightness. Specifically, stimuli that are more saturated (i.e. purer in colour) appear brighter than stimuli that are less saturated at the same luminance. Similarly, stimuli that are red or blue appear brighter than equiluminant yellow and green stimuli. This non-linear relationship between stimulus intensity and brightness, called the Helmholtz-Kohlrausch (HK) effect, was first described in the nineteenth century but has never been explained. Here, we take advantage of the relative simplicity of this ‘illusion’ to explain it and contextual effects more generally, by using a simple Bayesian ideal observer model of the human visual ecology. We also use fMRI brain scans to identify the neural correlates of brightness without changing the spatial context of the stimulus, which has complicated the interpretation of related fMRI studies.ResultsRather than modelling human vision directly, we use a Bayesian ideal observer to model human visual ecology. We show that the HK effect is a result of encoding the non-linear statistical relationship between retinal images and natural scenes that would have been experienced by the human visual system in the past. We further show that the complexity of this relationship is due to the response functions of the cone photoreceptors, which themselves are thought to represent an efficient solution to encoding the statistics of images. Finally, we show that the locus of the response to the relationship between images and scenes lies in the primary visual cortex (V1), if not earlier in the visual system, since the brightness of colours (as opposed to their luminance) accords with activity in V1 as measured with fMRI.ConclusionsThe data suggest that perceptions of brightness represent a robust visual response to the likely sources of stimuli, as determined, in this instance, by the known statistical relationship between scenes and their retinal responses. While the responses of the early visual system (receptors in this case) may represent specifically the statistics of images, post receptor responses are more likely represent the statistical relationship between images and scenes. A corollary of this suggestion is that the visual cortex is adapted to relate the retinal image to behaviour given the statistics of its past interactions with the sources of retinal images: the visual cortex is adapted to the signals it receives from the eyes, and not directly to the world beyond.

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Section: Discussionmentioning

confidence: 99%

The Brightness of Colour

Corney¹,

Haynes

Rees

et al. 2009

PLoS ONE

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“…Chromatic adaptation is considered the most important visual phenomenon when modelling colour appearance in humans (Fairchild, ). Even though mechanisms of chromatic adaptation may occur in higher stages of the visual system (in bees, see Lotto & Wicklein, ; in fishes, see Ingle, ) and may include cognitive processes in humans (Foster, ), the gain control of individual photoreceptors is an important mechanism of chromatic adaptation that likely occurs in most animals (Neumeyer, ; Kelber & Osorio, ). The von Kries transformation (von Kries, ) is the main algorithm used in models relevant to visual ecologists (for a test of other algorithms in bees, see Faruq, McOwan & Chittka, ).…”

Section: Classification Of Colour Spacesmentioning

confidence: 99%

Colour spaces in ecology and evolutionary biology

2015

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The recognition that animals sense the world in a different way than we do has unlocked important lines of research in ecology and evolutionary biology. In practice, the subjective study of natural stimuli has been permitted by perceptual spaces, which are graphical models of how stimuli are perceived by a given animal. Because colour vision is arguably the best-known sensory modality in most animals, a diversity of colour spaces are now available to visual ecologists, ranging from generalist and basic models allowing rough but robust predictions on colour perception, to species-specific, more complex models giving accurate but context-dependent predictions. Selecting among these models is most often influenced by historical contingencies that have associated models to specific questions and organisms; however, these associations are not always optimal. The aim of this review is to provide visual ecologists with a critical perspective on how models of colour space are built, how well they perform and where their main limitations are with regard to their most frequent uses in ecology and evolutionary biology. We propose a classification of models based on their complexity, defined as whether and how they model the mechanisms of chromatic adaptation and receptor opponency, the nonlinear association between the stimulus and its perception, and whether or not models have been fitted to experimental data. Then, we review the effect of modelling these mechanisms on predictions of colour detection and discrimination, colour conspicuousness, colour diversity and diversification, and for comparing the perception of colour traits between distinct perceivers. While a few rules emerge (e.g. opponent log-linear models should be preferred when analysing very distinct colours), in general model parameters still have poorly known effects. Colour spaces have nonetheless permitted significant advances in ecology and evolutionary biology, and more progress is expected if ecologists compare results between models and perform behavioural experiments more routinely. Such an approach would further contribute to a better understanding of colour vision and its links to the behavioural ecology of animals. While visual ecology is essentially a transfer of knowledge from visual sciences to evolutionary ecology, we hope that the discipline will benefit both fields more evenly in the future.

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“…On the one hand, we used light flux (photon counts cm -2 s -1 ) as a physical measurement (Menzel and Greggers, 1985;Werner et al, 1988;Lotto and Chittka, 2005;Lotto and Wicklein, 2005). On the other hand, we considered the spectral sensitivity curves reported for each photoreceptor type (Peitsch et al, 1992) to calculate photoreceptor excitations (photon catches) (Table2).…”

Section: Conditioned Stimulimentioning

confidence: 99%

Visual conditioning of the sting extension reflex in harnessed honeybees

Mota

Roussel

Sandoz

et al. 2011

Journal of Experimental Biology

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SUMMARYVisual performances of honeybees have been extensively studied using free-flying individuals trained to choose visual stimuli paired with sucrose reward. By contrast, harnessed bees in the laboratory were not thought to be capable of learning a Pavlovian association between a visual stimulus (CS) and sucrose reward (US). For reasons as yet unknown, harnessed bees only learn visual cues in association with sucrose if their antennae are ablated. However, slow acquisition and low retention performances are obtained in this case. Here, we established a novel visual conditioning protocol, which allows studying visual learning and memory in intact harnessed bees in the laboratory. This protocol consists of conditioning the sting extension reflex (SER) by pairing a visual stimulus (CS+) with an electric shock punishment (US), and a different visual stimulus (CS-) with the absence of shock. Bees with intact antennae learned the discrimination between CS+ and CS-by using chromatic cues, achromatic cues or both. Antennae ablation was not only unnecessary for learning to occur but it even impaired visual SER conditioning because of a concomitant reduction of responsiveness to the electric shock. We thus established the first visual conditioning protocol on harnessed honeybees that does not require injuring the experimental subjects. This novel experimental approach opens new doors for accessing the neural correlates of visual learning and memory in honeybees.

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Bees encode behaviorally significant spectral relationships in complex scenes to resolve stimulus ambiguity

Cited by 18 publications

References 18 publications

The Brightness of Colour

The Brightness of Colour

Colour spaces in ecology and evolutionary biology

Visual conditioning of the sting extension reflex in harnessed honeybees

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