Limits...
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.

Show MeSH

Related in: MedlinePlus

Structural plasticity of the lamina is controlled by the parallel action of a circadian clock and a phototransduction-dependent mechanism.a, Lamina volumes of adult wild-type CS (WT CS) flies kept under LL, LD, or DD conditions during adult life. All flies had experienced 12:12 LD cycles throughout larval and pupal development. The lamina volume oscillated in a circadian manner around a mean value which was larger in light-experienced flies than in dark-reared flies (F(2,1699)  = 156.7, p<0.0001, ANOVA). Sinusoidal-function fitting revealed a best fitting period of 23.7 h for LL (F(1,563) = 17.5, p<0.0001) and DD (F(1,515) = 5.6, p<0.05) lamina volume oscillations and 24.0 h for LD (F(1,621) = 34.2, p<0.0001). ‘Circadian Time’ (for LL and DD) ZT 0  =  light on, ZT 12  =  light off; for LL- and DD-flies read ZT as ‘Circadian Time’. b, Calculated amplitude deviations from the respective mean lamina volumes of all data points in a. Light experience significantly modified the time course of the circadian lamina-volume oscillations. This is most apparent at ZT 9, where LL reared flies showed the highest volume and DD reared flies the lowest volume. c, Lamina volumes of 10 to 15 adult mutant male flies per point of time kept under LL, LD or DD conditions. Circadian volume oscillations of the lamina were absent in the two clock mutants per01 and tim01 reared under LL- or DD-conditions. LD-reared animals displayed an increase in lamina volume during the day and a rapid decrease at night. The blind norpAP24 mutant displayed a robust circadian rhythm of lamina volumes. Under all rearing conditions the mean lamina volume rested at the DD-level of wild-type flies. d, Rescue of circadian lamina-volume oscillations in per01-mutants by the transgenic expression of PER-protein exclusively in photoreceptor cells R1-6 using per01; Rh1(−180)-per−1/+ flies. LD-reared R1-6-rescue flies displayed lamina-volume oscillations which were statistically indistinguishable in amplitude and time course from those of WT CS flies. Constant LL - or DD-conditions delayed the subjective day peaks by several hours in R1-6-rescued animals compared to wild-type flies. These observations are consistent with a previously described delay of the PER-protein cycle under DD-conditions in animals of the same genotype. For genetic reasons, in this experiment female flies were used. They were raised under LD-conditions up to their second day of adulthood before being reared for two more days in LL, LD or DD (n = 8 to 10 per point of time). Note that the overall lamina volume in females is higher than in males.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2821403&req=5

pone-0009217-g004: Structural plasticity of the lamina is controlled by the parallel action of a circadian clock and a phototransduction-dependent mechanism.a, Lamina volumes of adult wild-type CS (WT CS) flies kept under LL, LD, or DD conditions during adult life. All flies had experienced 12:12 LD cycles throughout larval and pupal development. The lamina volume oscillated in a circadian manner around a mean value which was larger in light-experienced flies than in dark-reared flies (F(2,1699)  = 156.7, p<0.0001, ANOVA). Sinusoidal-function fitting revealed a best fitting period of 23.7 h for LL (F(1,563) = 17.5, p<0.0001) and DD (F(1,515) = 5.6, p<0.05) lamina volume oscillations and 24.0 h for LD (F(1,621) = 34.2, p<0.0001). ‘Circadian Time’ (for LL and DD) ZT 0  =  light on, ZT 12  =  light off; for LL- and DD-flies read ZT as ‘Circadian Time’. b, Calculated amplitude deviations from the respective mean lamina volumes of all data points in a. Light experience significantly modified the time course of the circadian lamina-volume oscillations. This is most apparent at ZT 9, where LL reared flies showed the highest volume and DD reared flies the lowest volume. c, Lamina volumes of 10 to 15 adult mutant male flies per point of time kept under LL, LD or DD conditions. Circadian volume oscillations of the lamina were absent in the two clock mutants per01 and tim01 reared under LL- or DD-conditions. LD-reared animals displayed an increase in lamina volume during the day and a rapid decrease at night. The blind norpAP24 mutant displayed a robust circadian rhythm of lamina volumes. Under all rearing conditions the mean lamina volume rested at the DD-level of wild-type flies. d, Rescue of circadian lamina-volume oscillations in per01-mutants by the transgenic expression of PER-protein exclusively in photoreceptor cells R1-6 using per01; Rh1(−180)-per−1/+ flies. LD-reared R1-6-rescue flies displayed lamina-volume oscillations which were statistically indistinguishable in amplitude and time course from those of WT CS flies. Constant LL - or DD-conditions delayed the subjective day peaks by several hours in R1-6-rescued animals compared to wild-type flies. These observations are consistent with a previously described delay of the PER-protein cycle under DD-conditions in animals of the same genotype. For genetic reasons, in this experiment female flies were used. They were raised under LD-conditions up to their second day of adulthood before being reared for two more days in LL, LD or DD (n = 8 to 10 per point of time). Note that the overall lamina volume in females is higher than in males.

Mentions: Volumetric and behavioral data were fitted to a sinusoidal function (custom computer program by R. Wolf and M. Reif, Univ. Wuerzburg) followed by a least-square regression analysis to estimate whether the distribution of data better fits a sinusoidal curve or a flat line through the average of the data points (paired t-test). Subsequently, the data were fitted to sine waves of varying frequencies in order to determine the frequency with the best fit. In the corresponding figures (Fig. 3, 4, 5) we only present the best fit sine wave function.


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

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

Structural plasticity of the lamina is controlled by the parallel action of a circadian clock and a phototransduction-dependent mechanism.a, Lamina volumes of adult wild-type CS (WT CS) flies kept under LL, LD, or DD conditions during adult life. All flies had experienced 12:12 LD cycles throughout larval and pupal development. The lamina volume oscillated in a circadian manner around a mean value which was larger in light-experienced flies than in dark-reared flies (F(2,1699)  = 156.7, p<0.0001, ANOVA). Sinusoidal-function fitting revealed a best fitting period of 23.7 h for LL (F(1,563) = 17.5, p<0.0001) and DD (F(1,515) = 5.6, p<0.05) lamina volume oscillations and 24.0 h for LD (F(1,621) = 34.2, p<0.0001). ‘Circadian Time’ (for LL and DD) ZT 0  =  light on, ZT 12  =  light off; for LL- and DD-flies read ZT as ‘Circadian Time’. b, Calculated amplitude deviations from the respective mean lamina volumes of all data points in a. Light experience significantly modified the time course of the circadian lamina-volume oscillations. This is most apparent at ZT 9, where LL reared flies showed the highest volume and DD reared flies the lowest volume. c, Lamina volumes of 10 to 15 adult mutant male flies per point of time kept under LL, LD or DD conditions. Circadian volume oscillations of the lamina were absent in the two clock mutants per01 and tim01 reared under LL- or DD-conditions. LD-reared animals displayed an increase in lamina volume during the day and a rapid decrease at night. The blind norpAP24 mutant displayed a robust circadian rhythm of lamina volumes. Under all rearing conditions the mean lamina volume rested at the DD-level of wild-type flies. d, Rescue of circadian lamina-volume oscillations in per01-mutants by the transgenic expression of PER-protein exclusively in photoreceptor cells R1-6 using per01; Rh1(−180)-per−1/+ flies. LD-reared R1-6-rescue flies displayed lamina-volume oscillations which were statistically indistinguishable in amplitude and time course from those of WT CS flies. Constant LL - or DD-conditions delayed the subjective day peaks by several hours in R1-6-rescued animals compared to wild-type flies. These observations are consistent with a previously described delay of the PER-protein cycle under DD-conditions in animals of the same genotype. For genetic reasons, in this experiment female flies were used. They were raised under LD-conditions up to their second day of adulthood before being reared for two more days in LL, LD or DD (n = 8 to 10 per point of time). Note that the overall lamina volume in females is higher than in males.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0009217-g004: Structural plasticity of the lamina is controlled by the parallel action of a circadian clock and a phototransduction-dependent mechanism.a, Lamina volumes of adult wild-type CS (WT CS) flies kept under LL, LD, or DD conditions during adult life. All flies had experienced 12:12 LD cycles throughout larval and pupal development. The lamina volume oscillated in a circadian manner around a mean value which was larger in light-experienced flies than in dark-reared flies (F(2,1699)  = 156.7, p<0.0001, ANOVA). Sinusoidal-function fitting revealed a best fitting period of 23.7 h for LL (F(1,563) = 17.5, p<0.0001) and DD (F(1,515) = 5.6, p<0.05) lamina volume oscillations and 24.0 h for LD (F(1,621) = 34.2, p<0.0001). ‘Circadian Time’ (for LL and DD) ZT 0  =  light on, ZT 12  =  light off; for LL- and DD-flies read ZT as ‘Circadian Time’. b, Calculated amplitude deviations from the respective mean lamina volumes of all data points in a. Light experience significantly modified the time course of the circadian lamina-volume oscillations. This is most apparent at ZT 9, where LL reared flies showed the highest volume and DD reared flies the lowest volume. c, Lamina volumes of 10 to 15 adult mutant male flies per point of time kept under LL, LD or DD conditions. Circadian volume oscillations of the lamina were absent in the two clock mutants per01 and tim01 reared under LL- or DD-conditions. LD-reared animals displayed an increase in lamina volume during the day and a rapid decrease at night. The blind norpAP24 mutant displayed a robust circadian rhythm of lamina volumes. Under all rearing conditions the mean lamina volume rested at the DD-level of wild-type flies. d, Rescue of circadian lamina-volume oscillations in per01-mutants by the transgenic expression of PER-protein exclusively in photoreceptor cells R1-6 using per01; Rh1(−180)-per−1/+ flies. LD-reared R1-6-rescue flies displayed lamina-volume oscillations which were statistically indistinguishable in amplitude and time course from those of WT CS flies. Constant LL - or DD-conditions delayed the subjective day peaks by several hours in R1-6-rescued animals compared to wild-type flies. These observations are consistent with a previously described delay of the PER-protein cycle under DD-conditions in animals of the same genotype. For genetic reasons, in this experiment female flies were used. They were raised under LD-conditions up to their second day of adulthood before being reared for two more days in LL, LD or DD (n = 8 to 10 per point of time). Note that the overall lamina volume in females is higher than in males.
Mentions: Volumetric and behavioral data were fitted to a sinusoidal function (custom computer program by R. Wolf and M. Reif, Univ. Wuerzburg) followed by a least-square regression analysis to estimate whether the distribution of data better fits a sinusoidal curve or a flat line through the average of the data points (paired t-test). Subsequently, the data were fitted to sine waves of varying frequencies in order to determine the frequency with the best fit. In the corresponding figures (Fig. 3, 4, 5) we only present the best fit sine wave function.

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