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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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Sensitivity and dynamic range of optomotor behavior is controlled by experience-dependent and circadian mechanisms.a, b, LD-reared WT flies were behaviorally tested in the paradigms described in Fig. 2. Both, the sensitivity of the optomotor response at low light intensities (a, n>16 per point of time) and the dynamic range of optomotor behavior (b, n>30 per point of time) oscillated in a circadian, anti-phasic manner: highest behavioral sensitivity at night was accompanied by lowest dynamic range, and vice versa. c, Rescue of circadian oscillations in optomotor sensitivity by the restoration of the circadian clock in photoreceptor cells (Fig. 4d). Adult flies of the indicated genotypes were reared as described above and were behaviorally tested during their night- or day-phases (ZT 18–21 [set to 100%] and ZT 6–9, respectively). Irrespective of the genotype all LD-reared flies displayed a higher optomotor sensitivity during the night (F(1,74) = 14.6, p<0.0005). DD-reared wild-type flies as well as clock-rescued flies (per01; Rh1(−180)-per−1/+) showed a similar subjective day/night difference in behavioral sensitivity, which was absent in dark-reared per01-mutants. Error bars indicate s.e.m. values.
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pone-0009217-g005: Sensitivity and dynamic range of optomotor behavior is controlled by experience-dependent and circadian mechanisms.a, b, LD-reared WT flies were behaviorally tested in the paradigms described in Fig. 2. Both, the sensitivity of the optomotor response at low light intensities (a, n>16 per point of time) and the dynamic range of optomotor behavior (b, n>30 per point of time) oscillated in a circadian, anti-phasic manner: highest behavioral sensitivity at night was accompanied by lowest dynamic range, and vice versa. c, Rescue of circadian oscillations in optomotor sensitivity by the restoration of the circadian clock in photoreceptor cells (Fig. 4d). Adult flies of the indicated genotypes were reared as described above and were behaviorally tested during their night- or day-phases (ZT 18–21 [set to 100%] and ZT 6–9, respectively). Irrespective of the genotype all LD-reared flies displayed a higher optomotor sensitivity during the night (F(1,74) = 14.6, p<0.0005). DD-reared wild-type flies as well as clock-rescued flies (per01; Rh1(−180)-per−1/+) showed a similar subjective day/night difference in behavioral sensitivity, which was absent in dark-reared per01-mutants. Error bars indicate s.e.m. values.

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)

Sensitivity and dynamic range of optomotor behavior is controlled by experience-dependent and circadian mechanisms.a, b, LD-reared WT flies were behaviorally tested in the paradigms described in Fig. 2. Both, the sensitivity of the optomotor response at low light intensities (a, n>16 per point of time) and the dynamic range of optomotor behavior (b, n>30 per point of time) oscillated in a circadian, anti-phasic manner: highest behavioral sensitivity at night was accompanied by lowest dynamic range, and vice versa. c, Rescue of circadian oscillations in optomotor sensitivity by the restoration of the circadian clock in photoreceptor cells (Fig. 4d). Adult flies of the indicated genotypes were reared as described above and were behaviorally tested during their night- or day-phases (ZT 18–21 [set to 100%] and ZT 6–9, respectively). Irrespective of the genotype all LD-reared flies displayed a higher optomotor sensitivity during the night (F(1,74) = 14.6, p<0.0005). DD-reared wild-type flies as well as clock-rescued flies (per01; Rh1(−180)-per−1/+) showed a similar subjective day/night difference in behavioral sensitivity, which was absent in dark-reared per01-mutants. Error bars indicate s.e.m. values.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0009217-g005: Sensitivity and dynamic range of optomotor behavior is controlled by experience-dependent and circadian mechanisms.a, b, LD-reared WT flies were behaviorally tested in the paradigms described in Fig. 2. Both, the sensitivity of the optomotor response at low light intensities (a, n>16 per point of time) and the dynamic range of optomotor behavior (b, n>30 per point of time) oscillated in a circadian, anti-phasic manner: highest behavioral sensitivity at night was accompanied by lowest dynamic range, and vice versa. c, Rescue of circadian oscillations in optomotor sensitivity by the restoration of the circadian clock in photoreceptor cells (Fig. 4d). Adult flies of the indicated genotypes were reared as described above and were behaviorally tested during their night- or day-phases (ZT 18–21 [set to 100%] and ZT 6–9, respectively). Irrespective of the genotype all LD-reared flies displayed a higher optomotor sensitivity during the night (F(1,74) = 14.6, p<0.0005). DD-reared wild-type flies as well as clock-rescued flies (per01; Rh1(−180)-per−1/+) showed a similar subjective day/night difference in behavioral sensitivity, which was absent in dark-reared per01-mutants. Error bars indicate s.e.m. values.
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