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Circadian plasticity in photoreceptor cells controls visual coding efficiency in Drosophila melanogaster.

Barth M, Schultze M, Schuster CM, Strauss R - PLoS ONE (2010)

Bottom Line: Moreover, the sensory system of Drosophila cannot only account for predictable, but also for acute, environmental changes.The strength of a visually guided behavior, the optomotor turning response, co-varies with synaptic-terminal volume oscillations of photoreceptor cells when elicited at low light levels.Our results show that behaviorally relevant adaptive processing of visual information is performed, in part, at the level of visual input level.

View Article: PubMed Central - PubMed

Affiliation: Friedrich-Miescher-Laboratory of the Max-Planck Society (MPG), Tuebingen, Germany.

ABSTRACT
In the fly Drosophila melanogaster, neuronal plasticity of synaptic terminals in the first optic neuropil, or lamina, depends on early visual experience within a critical period after eclosion. The current study revealed two additional and parallel mechanisms involved in this type of synaptic terminal plasticity. First, an endogenous circadian rhythm causes daily oscillations in the volume of photoreceptor cell terminals. Second, daily visual experience precisely modulates the circadian time course and amplitude of the volume oscillations that the photoreceptor-cell terminals undergo. Both mechanisms are separable in their molecular basis. We suggest that the described neuronal plasticity in Drosophila ensures continuous optimal performance of the visual system over the course of a 24 h-day. Moreover, the sensory system of Drosophila cannot only account for predictable, but also for acute, environmental changes. The volumetric changes in the synaptic terminals of photoreceptor cells are accompanied by circadian and light-induced changes of presynaptic ribbons as well as extensions of epithelial glial cells into the photoreceptor terminals, suggesting that the architecture of the lamina is altered by both visual exposure and the circadian clock. Clock-mutant analysis and the rescue of PER protein rhythmicity exclusively in all R1-6 cells revealed that photoreceptor-cell plasticity is autonomous and sufficient to control visual behavior. The strength of a visually guided behavior, the optomotor turning response, co-varies with synaptic-terminal volume oscillations of photoreceptor cells when elicited at low light levels. Our results show that behaviorally relevant adaptive processing of visual information is performed, in part, at the level of visual input level.

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Model of parallel pathways.Light serves at least two functions in the visual system of Drosophila, it entrains and keeps the autonomous circadian clock of photoreceptors in phase and it triggers the phototransduction cascade. Both cellular mechanisms are active in parallel in photoreceptor cells and both converge in the volume control of their synaptic terminals in the lamina. The neuronal readout of this peripherally controlled morphological and functional plasticity is further computed downstream of the photoreceptor terminals, within the lamina and/or e.g. in the lobula plate, to instruct the appropriate behavior.
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pone-0009217-g006: Model of parallel pathways.Light serves at least two functions in the visual system of Drosophila, it entrains and keeps the autonomous circadian clock of photoreceptors in phase and it triggers the phototransduction cascade. Both cellular mechanisms are active in parallel in photoreceptor cells and both converge in the volume control of their synaptic terminals in the lamina. The neuronal readout of this peripherally controlled morphological and functional plasticity is further computed downstream of the photoreceptor terminals, within the lamina and/or e.g. in the lobula plate, to instruct the appropriate behavior.

Mentions: Our experiments show that volume plasticity of photoreceptor synaptic terminals is controlled by the parallel actions of both endogenous circadian- and vision-dependent mechanisms. As our genetic analyses suggest, the circadian input is independent from the phototransduction cascade and is synchronized by light/dark cycles. Visual input strongly depends on a functioning phototransduction cascade. We propose that both input pathways work in parallel and contribute to the period and phasing of the lamina oscillation and the absolute volume of the lamina (Fig. 6). The expression of the clock protein PER exclusively in the photoreceptor cells rescued both structural and behavioral circadian rhythmicity. Therefore, we conclude that the functioning circadian machinery in photoreceptor cells is sufficient to control visual coding efficiency in Drosophila. In addition, endothelial glia cells [25] and the large monopolar cells, L1 and L2 [9], [10] might contribute to the output of this circadian network. The specificity of the observed plasticity in the first optic neuropil suggests that this plasticity might participate in the transduction and processing of primary sensory signals rather than in direct photoreception. Our findings do not exclude the possibility, however, that the autonomous network in the periphery of the visual system is affected by circadian oscillators in other parts of the brain such as the axonal terminals of the PDF circuit [11; for large flies: 9], although we have no indication that this is the case.


Circadian plasticity in photoreceptor cells controls visual coding efficiency in Drosophila melanogaster.

Barth M, Schultze M, Schuster CM, Strauss R - PLoS ONE (2010)

Model of parallel pathways.Light serves at least two functions in the visual system of Drosophila, it entrains and keeps the autonomous circadian clock of photoreceptors in phase and it triggers the phototransduction cascade. Both cellular mechanisms are active in parallel in photoreceptor cells and both converge in the volume control of their synaptic terminals in the lamina. The neuronal readout of this peripherally controlled morphological and functional plasticity is further computed downstream of the photoreceptor terminals, within the lamina and/or e.g. in the lobula plate, to instruct the appropriate behavior.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2821403&req=5

pone-0009217-g006: Model of parallel pathways.Light serves at least two functions in the visual system of Drosophila, it entrains and keeps the autonomous circadian clock of photoreceptors in phase and it triggers the phototransduction cascade. Both cellular mechanisms are active in parallel in photoreceptor cells and both converge in the volume control of their synaptic terminals in the lamina. The neuronal readout of this peripherally controlled morphological and functional plasticity is further computed downstream of the photoreceptor terminals, within the lamina and/or e.g. in the lobula plate, to instruct the appropriate behavior.
Mentions: Our experiments show that volume plasticity of photoreceptor synaptic terminals is controlled by the parallel actions of both endogenous circadian- and vision-dependent mechanisms. As our genetic analyses suggest, the circadian input is independent from the phototransduction cascade and is synchronized by light/dark cycles. Visual input strongly depends on a functioning phototransduction cascade. We propose that both input pathways work in parallel and contribute to the period and phasing of the lamina oscillation and the absolute volume of the lamina (Fig. 6). The expression of the clock protein PER exclusively in the photoreceptor cells rescued both structural and behavioral circadian rhythmicity. Therefore, we conclude that the functioning circadian machinery in photoreceptor cells is sufficient to control visual coding efficiency in Drosophila. In addition, endothelial glia cells [25] and the large monopolar cells, L1 and L2 [9], [10] might contribute to the output of this circadian network. The specificity of the observed plasticity in the first optic neuropil suggests that this plasticity might participate in the transduction and processing of primary sensory signals rather than in direct photoreception. Our findings do not exclude the possibility, however, that the autonomous network in the periphery of the visual system is affected by circadian oscillators in other parts of the brain such as the axonal terminals of the PDF circuit [11; for large flies: 9], although we have no indication that this is the case.

Bottom Line: Moreover, the sensory system of Drosophila cannot only account for predictable, but also for acute, environmental changes.The strength of a visually guided behavior, the optomotor turning response, co-varies with synaptic-terminal volume oscillations of photoreceptor cells when elicited at low light levels.Our results show that behaviorally relevant adaptive processing of visual information is performed, in part, at the level of visual input level.

View Article: PubMed Central - PubMed

Affiliation: Friedrich-Miescher-Laboratory of the Max-Planck Society (MPG), Tuebingen, Germany.

ABSTRACT
In the fly Drosophila melanogaster, neuronal plasticity of synaptic terminals in the first optic neuropil, or lamina, depends on early visual experience within a critical period after eclosion. The current study revealed two additional and parallel mechanisms involved in this type of synaptic terminal plasticity. First, an endogenous circadian rhythm causes daily oscillations in the volume of photoreceptor cell terminals. Second, daily visual experience precisely modulates the circadian time course and amplitude of the volume oscillations that the photoreceptor-cell terminals undergo. Both mechanisms are separable in their molecular basis. We suggest that the described neuronal plasticity in Drosophila ensures continuous optimal performance of the visual system over the course of a 24 h-day. Moreover, the sensory system of Drosophila cannot only account for predictable, but also for acute, environmental changes. The volumetric changes in the synaptic terminals of photoreceptor cells are accompanied by circadian and light-induced changes of presynaptic ribbons as well as extensions of epithelial glial cells into the photoreceptor terminals, suggesting that the architecture of the lamina is altered by both visual exposure and the circadian clock. Clock-mutant analysis and the rescue of PER protein rhythmicity exclusively in all R1-6 cells revealed that photoreceptor-cell plasticity is autonomous and sufficient to control visual behavior. The strength of a visually guided behavior, the optomotor turning response, co-varies with synaptic-terminal volume oscillations of photoreceptor cells when elicited at low light levels. Our results show that behaviorally relevant adaptive processing of visual information is performed, in part, at the level of visual input level.

Show MeSH
Related in: MedlinePlus