Spotlight on the evolution of vision

Colley, Nansi Jo; Dowling, John E.

doi:10.1017/s0952523813000059

Cited by 11 publications

(6 citation statements)

References 35 publications

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“…Anatomical evidence suggests they do: S cones may enter MT by way of diffuse bipolar cells (Dacey & Lee, 1994; Dacey, 1996; Calkins et al , 1998; Klug et al , 2003; Percival et al , 2009), which provide the excitatory input to parasol ganglion cells and LGN magnocellular cells. This evidence implies that diffuse bipolar cells and magnocellular cells should respond to S-cone-isolating stimuli, but physiological studies have not been able to confirm this prediction conclusively (Derrington et al , 1984; Chatterjee & Callaway, 2002; Reid & Shapley, 2002; Sun et al , 2006; Dacey et al , 2013). A surprising piece of evidence in favor of S-cone input to MT comes from other anatomical work.…”

Section: Mtmentioning

confidence: 91%

Color signals through dorsal and ventral visual pathways

Conway

2013

Vis Neurosci

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Explanations for color phenomena are often sought in the retina, LGN and V1, yet it is becoming increasingly clear that a complete account will take us further along the visual-processing pathway. Working out which areas are involved is not trivial. Responses to S-cone activation are often assumed to indicate that an area or neuron is involved in color perception. However, work tracing S-cone signals into extrastriate cortex has challenged this assumption: S-cone responses have been found in brain regions, such as MT, not thought to play a major role in color perception. Here we review the processing of S-cone signals across cortex and present original data on S-cone responses measured with fMRI in alert macaque, focusing on one area in which S-cone signals seem likely to contribute to color (V4/posterior inferior temporal cortex), and on one area in which S signals are unlikely to play a role in color (MT). We advance a hypothesis that the S-cone signals in color-computing areas are required to achieve a balanced neural representation of perceptual color space, while the S-cone signals in non-color-areas provide a cue to illumination (not luminance) and confer sensitivity to the chromatic contrast generated by natural daylight (shadows, illuminated by ambient sky, surrounded by direct sunlight). This sensitivity would facilitate the extraction of shape-from-shadow signals to benefit global scene analysis and motion perception.

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Section: Mtmentioning

confidence: 91%

Color signals through dorsal and ventral visual pathways

Conway

2013

Vis Neurosci

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“…Alternatively, R8 and R7 are known to synapse on each other and spectral opponency in Drosophila could arise at the level of the photoreceptors themselves, as suggested previously for butterflies (Takemura et al, 2008; Takemura & Arikawa, 2006). Primate S cones have recently been shown to get opponent inputs from horizontal cells (Packer et al, 2010; Dacey et al, 2013) and generate blue-yellow opponent responses, while in ground squirrels, a specific amacrine type provides a blue-OFF signal to the blue/yellow opponent ganglion cells (Chen & Li, 2012). Alternatively, spectral opponency could arise downstream of these medulla projection neurons, or these cells might implement spectral pre-processing filters that are hypothesized to form the basis of simple color constancy (van Hateren, 1993).…”

Section: Discussionmentioning

confidence: 99%

Multiple Redundant Medulla Projection Neurons Mediate Color Vision inDrosophila

Melnattur

Pursley

Lin

et al. 2014

Journal of Neurogenetics

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The receptor mechanism for color vision has been extensively studied. In contrast, the circuit(s) that transform(s) photoreceptor signals into color percepts to guide behavior remain(s) poorly characterized. Using intersectional genetics to inactivate identified subsets of neurons, we have uncovered the first-order interneurons that are functionally required for hue discrimination in Drosophila. We developed a novel aversive operant conditioning assay for intensity independent color discrimination (true color vision) in Drosophila. Single flying flies are magnetically tethered in an arena surrounded by blue and green LEDs. The flies’ optomotor response is used to determine the blue-green isoluminant intensity. Flies are then conditioned to discriminate between equiluminant blue or green stimuli. Wild-type flies are successfully trained in this paradigm when conditioned to avoid either blue or green. Functional color entrainment requires the function of the narrow spectrum photoreceptors R8 and/or R7, and is within a limited range, intensity independent, suggesting that it is mediated by a color vision system. The medulla projection neurons, Tm5a/b/c and Tm20, receive direct inputs from R7 or R8 photoreceptors and indirect input from the broad spectrum photoreceptors R1-R6 via the lamina neuron L3. Genetically inactivating these four classes of medulla projection neurons abolished color learning. However, inactivation of subsets of these neurons is insufficient to block color learning, suggesting that true color vision is mediated by multiple redundant pathways. We hypothesize that flies represent color along multiple axes at the first synapse in the fly visual system. The apparent redundancy in learned color discrimination sharply contrasts with innate UV spectral preference, which is dominated by a single pathway from the amacrine neuron Dm8 to the Tm5c projection neurons.

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“…For opsins to work continuously, there must be an efficient mechanism for reconverting the all- trans state of retinal to its original 11- cis form. In the c-opsins of vertebrates, all- trans retinal dissociates from the opsin molecule and is reconverted to 11- cis through a complex process of transport and enzyme conversion (Kusakabe et al, 2009; Goldsmith, 2013). Insect r-opsins are instead bi-stable, such that the opsin can hold both isoforms of retinal, and reconversion is accomplished by the absorption of yet another photon.…”

Section: The Origin and Diversification Of Photoreceptionmentioning

confidence: 99%

Eye evolution and its functional basis

2013

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Eye evolution is driven by the evolution of visually guided behavior. Accumulation of gradually more demanding behaviors have continuously increased the performance requirements on the photoreceptor organs. Starting with nondirectional photoreception, I argue for an evolutionary sequence continuing with directional photoreception, low-resolution vision, and finally, high-resolution vision. Calculations of the physical requirements for these four sensory tasks show that they correlate with major innovations in eye evolution and thus work as a relevant classification for a functional analysis of eye evolution. Together with existing molecular and morphological data, the functional analysis suggests that urbilateria had a simple set of rhabdomeric and ciliary receptors used for directional photoreception, and that organ duplications, positional shifts and functional shifts account for the diverse patterns of eyes and photoreceptors seen in extant animals. The analysis also suggests that directional photoreception evolved independently at least twice before the last common ancestor of bilateria and proceeded several times independently to true vision in different bilaterian and cnidarian groups. This scenario is compatible with Pax-gene expression in eye development in the different animal groups. The whole process from the first opsin to high-resolution vision took about 170 million years and was largely completed by the onset of the Cambrian, about 530 million years ago. Evolution from shadow detectors to multiple directional photoreceptors has further led to secondary cases of eye evolution in bivalves, fan worms, and chitons.

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Spotlight on the evolution of vision

Cited by 11 publications

References 35 publications

Color signals through dorsal and ventral visual pathways

Color signals through dorsal and ventral visual pathways

Multiple Redundant Medulla Projection Neurons Mediate Color Vision inDrosophila

Eye evolution and its functional basis

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