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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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Experience-dependent plasticity in the lamina of wild-type Drosophila melanogaster.a, Autofluorescence profiles of the lamina neuropil (La) from adult flies reared for four days in constant darkness (DD) or constant light (LL; flies were fixed at ZT 6). Note the gross morphological size changes of the laminae. b, Electron-micrographs of distal lamina sections of flies sectioned at day and night. Six synaptic terminals of photoreceptor cells (R) converge on to two Large Monopolar Cells (L), forming the so called cartridge. Scale bar, 1 µm. c, Significant differences between LL- (white columns) and DD-flies (black columns) were found for lamina volume, cross-sectional area of the photoreceptor terminals (1/6 hatched in b), circumference of the membrane surrounding these terminals (1/6 dotted line in b) and presynaptic T-bars residing on this membrane. Spacing between neighboring synapses was statistically indistinguishable. Finally, in LL-flies more shallow capitate projections were found, whereas in DD-flies more deep capitate projections invaded the photoreceptor terminals. Number of presynaptic T-bars and capitate projections were counted per section. Error bars denote s.e.m. values.
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pone-0009217-g001: Experience-dependent plasticity in the lamina of wild-type Drosophila melanogaster.a, Autofluorescence profiles of the lamina neuropil (La) from adult flies reared for four days in constant darkness (DD) or constant light (LL; flies were fixed at ZT 6). Note the gross morphological size changes of the laminae. b, Electron-micrographs of distal lamina sections of flies sectioned at day and night. Six synaptic terminals of photoreceptor cells (R) converge on to two Large Monopolar Cells (L), forming the so called cartridge. Scale bar, 1 µm. c, Significant differences between LL- (white columns) and DD-flies (black columns) were found for lamina volume, cross-sectional area of the photoreceptor terminals (1/6 hatched in b), circumference of the membrane surrounding these terminals (1/6 dotted line in b) and presynaptic T-bars residing on this membrane. Spacing between neighboring synapses was statistically indistinguishable. Finally, in LL-flies more shallow capitate projections were found, whereas in DD-flies more deep capitate projections invaded the photoreceptor terminals. Number of presynaptic T-bars and capitate projections were counted per section. Error bars denote s.e.m. values.

Mentions: In the fruit fly, Drosophila melanogaster, and in other insect species, the first optic neuropil, or lamina, is a potential site for such adaptive neuronal coding. It was reported that visual stimulation early in adult life increases the size of both optic lobes in Drosophila melanogaster [1] and certain brain regions [4], suggesting that visual experience during a critical period is involved in fine-tuning the development of neuronal circuitry. Specifically, the lamina is largest in flies reared in constant light (LL) and smallest in those reared in constant darkness (DD; see also Fig. 1a). These gross morphological changes are accompanied by corresponding volume differences in photoreceptor cell terminals [3]. In addition to this earlier investigation, we now studied also the frequency of presynaptic ribbons [5] and extensions of epithelia glial cells [deep and shallow capitate projections; 6], [7] into or onto the photoreceptor cell terminals. Altogether, the results of this investigation lead to the assumption that not only is the volume of photoreceptor cell terminals highly modifiable, but so is the whole neuronal architecture of the lamina of Drosophila melanogaster.


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

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

Experience-dependent plasticity in the lamina of wild-type Drosophila melanogaster.a, Autofluorescence profiles of the lamina neuropil (La) from adult flies reared for four days in constant darkness (DD) or constant light (LL; flies were fixed at ZT 6). Note the gross morphological size changes of the laminae. b, Electron-micrographs of distal lamina sections of flies sectioned at day and night. Six synaptic terminals of photoreceptor cells (R) converge on to two Large Monopolar Cells (L), forming the so called cartridge. Scale bar, 1 µm. c, Significant differences between LL- (white columns) and DD-flies (black columns) were found for lamina volume, cross-sectional area of the photoreceptor terminals (1/6 hatched in b), circumference of the membrane surrounding these terminals (1/6 dotted line in b) and presynaptic T-bars residing on this membrane. Spacing between neighboring synapses was statistically indistinguishable. Finally, in LL-flies more shallow capitate projections were found, whereas in DD-flies more deep capitate projections invaded the photoreceptor terminals. Number of presynaptic T-bars and capitate projections were counted per section. Error bars denote s.e.m. values.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0009217-g001: Experience-dependent plasticity in the lamina of wild-type Drosophila melanogaster.a, Autofluorescence profiles of the lamina neuropil (La) from adult flies reared for four days in constant darkness (DD) or constant light (LL; flies were fixed at ZT 6). Note the gross morphological size changes of the laminae. b, Electron-micrographs of distal lamina sections of flies sectioned at day and night. Six synaptic terminals of photoreceptor cells (R) converge on to two Large Monopolar Cells (L), forming the so called cartridge. Scale bar, 1 µm. c, Significant differences between LL- (white columns) and DD-flies (black columns) were found for lamina volume, cross-sectional area of the photoreceptor terminals (1/6 hatched in b), circumference of the membrane surrounding these terminals (1/6 dotted line in b) and presynaptic T-bars residing on this membrane. Spacing between neighboring synapses was statistically indistinguishable. Finally, in LL-flies more shallow capitate projections were found, whereas in DD-flies more deep capitate projections invaded the photoreceptor terminals. Number of presynaptic T-bars and capitate projections were counted per section. Error bars denote s.e.m. values.
Mentions: In the fruit fly, Drosophila melanogaster, and in other insect species, the first optic neuropil, or lamina, is a potential site for such adaptive neuronal coding. It was reported that visual stimulation early in adult life increases the size of both optic lobes in Drosophila melanogaster [1] and certain brain regions [4], suggesting that visual experience during a critical period is involved in fine-tuning the development of neuronal circuitry. Specifically, the lamina is largest in flies reared in constant light (LL) and smallest in those reared in constant darkness (DD; see also Fig. 1a). These gross morphological changes are accompanied by corresponding volume differences in photoreceptor cell terminals [3]. In addition to this earlier investigation, we now studied also the frequency of presynaptic ribbons [5] and extensions of epithelia glial cells [deep and shallow capitate projections; 6], [7] into or onto the photoreceptor cell terminals. Altogether, the results of this investigation lead to the assumption that not only is the volume of photoreceptor cell terminals highly modifiable, but so is the whole neuronal architecture of the lamina of Drosophila melanogaster.

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