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A Stochastic Burst Follows the Periodic Morning Peak in Individual Drosophila Locomotion.

Lazopulo S, Lopez JA, Levy P, Syed S - PLoS ONE (2015)

Bottom Line: In a single fly recording, the burst is likely to appear once randomly within 0.5-5 hours after lights turn on, last for only 2-3 minutes and yet show 5 times greater activity compared to the maximum of morning peak with data binned in 3 minutes.Additionally, we find that genetic ablation of the clock has insignificant effect on burst frequency.Together, these data suggest that the pronounced burst is likely generated by a light-activated circuit that is independent of the circadian clock.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, University of Miami, Coral Gables, Florida, United States of America.

ABSTRACT
Coupling between cyclically varying external light and an endogenous biochemical oscillator known as the circadian clock, modulates a rhythmic pattern with two prominent peaks in the locomotion of Drosophila melanogaster. A morning peak appears around the time lights turn on and an evening peak appears just before lights turn off. The close association between the peaks and the external 12:12 hour light/dark photoperiod means that respective morning and evening peaks of individual flies are well-synchronized in time and, consequently, feature prominently in population-averaged data. Here, we report on a brief but strong stochastic burst in fly activity that, in contrast to morning and evening peaks, is detectable only in single fly recordings. This burst was observed across 3 wild-type strains of Drosophila melanogaster. In a single fly recording, the burst is likely to appear once randomly within 0.5-5 hours after lights turn on, last for only 2-3 minutes and yet show 5 times greater activity compared to the maximum of morning peak with data binned in 3 minutes. Owing to its variable timing and short duration, the burst is virtually undetectable in population-averaged data. We use a locally-built illumination system to study the burst and find that its incidence in a population correlates with light intensity, with ~85% of control flies showing the behavior at 8000 lux (1942 μW/cm2). Consistent with that finding, several mutant flies with impaired vision show substantially reduced frequency of the burst. Additionally, we find that genetic ablation of the clock has insignificant effect on burst frequency. Together, these data suggest that the pronounced burst is likely generated by a light-activated circuit that is independent of the circadian clock.

No MeSH data available.


Related in: MedlinePlus

Locomotor activity at different light intensities.Population-averaged activity profiles of iso31 (panel A, left) and yw (panel A, right) for different midday light levels. Only yw shows appearance of the A-peak for ~8000 lux. (B) Cartoon of the peak properties plotted in C-G. iso31 flies shown in black circles and yw flies in white triangles, grey solid and dashed curves are guides to the eye. The midday activity (C) is an average activity of 4 hours from 4 to 8 hours after lights-on. It increases with light intensity for both fly strains. (D) Half-width of the M peak increases while (E) half-width of the E peak decreases with light intensity. Areas of M and E peaks (F and G) represent total activity from 3 hours before to 3 hours after respective peak. With the exception of the E-peak of iso31, areas under the peaks increase with increase in light intensity. Legend in (C) applies to panels C-G.
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pone.0140481.g002: Locomotor activity at different light intensities.Population-averaged activity profiles of iso31 (panel A, left) and yw (panel A, right) for different midday light levels. Only yw shows appearance of the A-peak for ~8000 lux. (B) Cartoon of the peak properties plotted in C-G. iso31 flies shown in black circles and yw flies in white triangles, grey solid and dashed curves are guides to the eye. The midday activity (C) is an average activity of 4 hours from 4 to 8 hours after lights-on. It increases with light intensity for both fly strains. (D) Half-width of the M peak increases while (E) half-width of the E peak decreases with light intensity. Areas of M and E peaks (F and G) represent total activity from 3 hours before to 3 hours after respective peak. With the exception of the E-peak of iso31, areas under the peaks increase with increase in light intensity. Legend in (C) applies to panels C-G.

Mentions: To further investigate differences in the locomotor behavior of control strains, we next studied yw and iso31 flies using trapezoidal light cycle, which features a linear change in light levels around dawn and dusk. The ramp rate between zero and the maximum was varied depending on the maximum lux target such that the increase/decrease always took one hour. For both strains, population-averaged analyses show presence of M and E peaks for all days (Fig 2A). In iso31, high light levels produce extended morning activity, resulting in flies being active throughout the middle of the day. In contrast, in yw flies high light levels instead produce the ‘A’ peak around ZT 6 (Fig 2A). Our observation that the A peak appears with increasing illumination is consistent with results reported by De et. al. [15] and at odds with that of Vanin et. al. who attributed appearance of the peak to temperature oscillations in the environment [13]. Although different in terms of the A peak, both iso31 and yw flies show increase in midday activity with increase in light levels (Fig 2C). The response rates are, however, different and likely related to the midday A peak being present only in yw flies (Fig 2C solid and dashed lines). The two strains also show differences in how their M and E activity peaks respond to changes in light. The data show that while both the half-width and the area of the M peak increase with illumination (Fig 2D and 2F), half-width of the E peak paradoxically decreases with higher light intensities (Fig 2E). The monotonic decrease in half-width of the E peak with increasing light intensity (Fig 2E) maybe reminiscent of the previously reported light-sensitive contribution of DN1 cells to the evening peak [10]. Because of this narrowing of the E peak, its area also decreases in iso31, but not in yw (Fig 2G). These population-averaged data reveal significant differences in light response by the M and E activity peaks. The differences between the peaks may reflect differences in sensitivity of the underlying M and E cells that generate activity. Additionally, the data show dissimilarities in locomotor patterns between two commonly used fly strains, underscoring the importance of genetic background in behavior [31].


A Stochastic Burst Follows the Periodic Morning Peak in Individual Drosophila Locomotion.

Lazopulo S, Lopez JA, Levy P, Syed S - PLoS ONE (2015)

Locomotor activity at different light intensities.Population-averaged activity profiles of iso31 (panel A, left) and yw (panel A, right) for different midday light levels. Only yw shows appearance of the A-peak for ~8000 lux. (B) Cartoon of the peak properties plotted in C-G. iso31 flies shown in black circles and yw flies in white triangles, grey solid and dashed curves are guides to the eye. The midday activity (C) is an average activity of 4 hours from 4 to 8 hours after lights-on. It increases with light intensity for both fly strains. (D) Half-width of the M peak increases while (E) half-width of the E peak decreases with light intensity. Areas of M and E peaks (F and G) represent total activity from 3 hours before to 3 hours after respective peak. With the exception of the E-peak of iso31, areas under the peaks increase with increase in light intensity. Legend in (C) applies to panels C-G.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4631454&req=5

pone.0140481.g002: Locomotor activity at different light intensities.Population-averaged activity profiles of iso31 (panel A, left) and yw (panel A, right) for different midday light levels. Only yw shows appearance of the A-peak for ~8000 lux. (B) Cartoon of the peak properties plotted in C-G. iso31 flies shown in black circles and yw flies in white triangles, grey solid and dashed curves are guides to the eye. The midday activity (C) is an average activity of 4 hours from 4 to 8 hours after lights-on. It increases with light intensity for both fly strains. (D) Half-width of the M peak increases while (E) half-width of the E peak decreases with light intensity. Areas of M and E peaks (F and G) represent total activity from 3 hours before to 3 hours after respective peak. With the exception of the E-peak of iso31, areas under the peaks increase with increase in light intensity. Legend in (C) applies to panels C-G.
Mentions: To further investigate differences in the locomotor behavior of control strains, we next studied yw and iso31 flies using trapezoidal light cycle, which features a linear change in light levels around dawn and dusk. The ramp rate between zero and the maximum was varied depending on the maximum lux target such that the increase/decrease always took one hour. For both strains, population-averaged analyses show presence of M and E peaks for all days (Fig 2A). In iso31, high light levels produce extended morning activity, resulting in flies being active throughout the middle of the day. In contrast, in yw flies high light levels instead produce the ‘A’ peak around ZT 6 (Fig 2A). Our observation that the A peak appears with increasing illumination is consistent with results reported by De et. al. [15] and at odds with that of Vanin et. al. who attributed appearance of the peak to temperature oscillations in the environment [13]. Although different in terms of the A peak, both iso31 and yw flies show increase in midday activity with increase in light levels (Fig 2C). The response rates are, however, different and likely related to the midday A peak being present only in yw flies (Fig 2C solid and dashed lines). The two strains also show differences in how their M and E activity peaks respond to changes in light. The data show that while both the half-width and the area of the M peak increase with illumination (Fig 2D and 2F), half-width of the E peak paradoxically decreases with higher light intensities (Fig 2E). The monotonic decrease in half-width of the E peak with increasing light intensity (Fig 2E) maybe reminiscent of the previously reported light-sensitive contribution of DN1 cells to the evening peak [10]. Because of this narrowing of the E peak, its area also decreases in iso31, but not in yw (Fig 2G). These population-averaged data reveal significant differences in light response by the M and E activity peaks. The differences between the peaks may reflect differences in sensitivity of the underlying M and E cells that generate activity. Additionally, the data show dissimilarities in locomotor patterns between two commonly used fly strains, underscoring the importance of genetic background in behavior [31].

Bottom Line: In a single fly recording, the burst is likely to appear once randomly within 0.5-5 hours after lights turn on, last for only 2-3 minutes and yet show 5 times greater activity compared to the maximum of morning peak with data binned in 3 minutes.Additionally, we find that genetic ablation of the clock has insignificant effect on burst frequency.Together, these data suggest that the pronounced burst is likely generated by a light-activated circuit that is independent of the circadian clock.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, University of Miami, Coral Gables, Florida, United States of America.

ABSTRACT
Coupling between cyclically varying external light and an endogenous biochemical oscillator known as the circadian clock, modulates a rhythmic pattern with two prominent peaks in the locomotion of Drosophila melanogaster. A morning peak appears around the time lights turn on and an evening peak appears just before lights turn off. The close association between the peaks and the external 12:12 hour light/dark photoperiod means that respective morning and evening peaks of individual flies are well-synchronized in time and, consequently, feature prominently in population-averaged data. Here, we report on a brief but strong stochastic burst in fly activity that, in contrast to morning and evening peaks, is detectable only in single fly recordings. This burst was observed across 3 wild-type strains of Drosophila melanogaster. In a single fly recording, the burst is likely to appear once randomly within 0.5-5 hours after lights turn on, last for only 2-3 minutes and yet show 5 times greater activity compared to the maximum of morning peak with data binned in 3 minutes. Owing to its variable timing and short duration, the burst is virtually undetectable in population-averaged data. We use a locally-built illumination system to study the burst and find that its incidence in a population correlates with light intensity, with ~85% of control flies showing the behavior at 8000 lux (1942 μW/cm2). Consistent with that finding, several mutant flies with impaired vision show substantially reduced frequency of the burst. Additionally, we find that genetic ablation of the clock has insignificant effect on burst frequency. Together, these data suggest that the pronounced burst is likely generated by a light-activated circuit that is independent of the circadian clock.

No MeSH data available.


Related in: MedlinePlus