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Sensory Conflict Disrupts Activity of the Drosophila Circadian Network

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ABSTRACT

Periodic changes in light and temperature synchronize the Drosophila circadian clock, but the question of how the fly brain integrates these two input pathways to set circadian time remains unanswered. We explore multisensory cue combination by testing the resilience of the circadian network to conflicting environmental inputs. We show that misaligned light and temperature cycles can lead to dramatic changes in the daily locomotor activities of wild-type flies during and after exposure to sensory conflict. This altered behavior is associated with a drastic reduction in the amplitude of PERIOD (PER) oscillations in brain clock neurons and desynchronization between light- and temperature-sensitive neuronal subgroups. The behavioral disruption depends heavily on the phase relationship between light and temperature signals. Our results represent a systematic quantification of multisensory integration in the Drosophila circadian system and lend further support to the view of the clock as a network of coupled oscillatory subunits.

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Behavioral Responses to Different Light and Temperature Phase RelationshipsVarying degrees of LD:TC misalignments in wild-type (A and B) and cry02 flies (C and D) (45 ≤ n ≤ 65). (A and C) Representative days of locomotor behavior taken from average actograms during conflict conditions after activity rhythms had stabilized (part III, days 5–6). (C and D) Gradients of linear regression fit to the period of activity preceding light and temperature cutoffs. Shaded regions denote 95% confidence intervals. Black cross indicates gradient of evening activity during corresponding in-phase condition (see also Figure S4).
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fig4: Behavioral Responses to Different Light and Temperature Phase RelationshipsVarying degrees of LD:TC misalignments in wild-type (A and B) and cry02 flies (C and D) (45 ≤ n ≤ 65). (A and C) Representative days of locomotor behavior taken from average actograms during conflict conditions after activity rhythms had stabilized (part III, days 5–6). (C and D) Gradients of linear regression fit to the period of activity preceding light and temperature cutoffs. Shaded regions denote 95% confidence intervals. Black cross indicates gradient of evening activity during corresponding in-phase condition (see also Figure S4).

Mentions: By contrast, during conflict, we observed a striking collapse in the amplitude of PER oscillations for all neuronal subgroups in wild-type flies (Figures 2A, right, 2C, bottom, and 2D). Furthermore, inspecting the residual low-amplitude PER oscillations, there appeared to be a clear shift in the peak of the s-LNv, l-LNv, LNd, and DN1 to ZTL21, suggesting at least partial entrainment of these neurons to LD. In contrast, the CRY-negative DN2 and DN3 remained phase-locked to TC, displaying peak PER expression at ZTT21. We did not notice any obvious phase heterogeneity within each neuronal subgroup (see, for example, the DN2 and LNd in Figure 4C). In cry02 mutants under conflict conditions, molecular rhythms remained comparable to part I (Figures 2B, right, 2D). This echoes our behavioral findings, suggesting that the altered molecular rhythms observed in wild-type flies result from the integration of conflicting inputs to the clock network, and that such conflicts can be avoided by weakening one of the input pathways, as in cry02 mutants.


Sensory Conflict Disrupts Activity of the Drosophila Circadian Network
Behavioral Responses to Different Light and Temperature Phase RelationshipsVarying degrees of LD:TC misalignments in wild-type (A and B) and cry02 flies (C and D) (45 ≤ n ≤ 65). (A and C) Representative days of locomotor behavior taken from average actograms during conflict conditions after activity rhythms had stabilized (part III, days 5–6). (C and D) Gradients of linear regression fit to the period of activity preceding light and temperature cutoffs. Shaded regions denote 95% confidence intervals. Black cross indicates gradient of evening activity during corresponding in-phase condition (see also Figure S4).
© Copyright Policy - CC BY
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5120367&req=5

fig4: Behavioral Responses to Different Light and Temperature Phase RelationshipsVarying degrees of LD:TC misalignments in wild-type (A and B) and cry02 flies (C and D) (45 ≤ n ≤ 65). (A and C) Representative days of locomotor behavior taken from average actograms during conflict conditions after activity rhythms had stabilized (part III, days 5–6). (C and D) Gradients of linear regression fit to the period of activity preceding light and temperature cutoffs. Shaded regions denote 95% confidence intervals. Black cross indicates gradient of evening activity during corresponding in-phase condition (see also Figure S4).
Mentions: By contrast, during conflict, we observed a striking collapse in the amplitude of PER oscillations for all neuronal subgroups in wild-type flies (Figures 2A, right, 2C, bottom, and 2D). Furthermore, inspecting the residual low-amplitude PER oscillations, there appeared to be a clear shift in the peak of the s-LNv, l-LNv, LNd, and DN1 to ZTL21, suggesting at least partial entrainment of these neurons to LD. In contrast, the CRY-negative DN2 and DN3 remained phase-locked to TC, displaying peak PER expression at ZTT21. We did not notice any obvious phase heterogeneity within each neuronal subgroup (see, for example, the DN2 and LNd in Figure 4C). In cry02 mutants under conflict conditions, molecular rhythms remained comparable to part I (Figures 2B, right, 2D). This echoes our behavioral findings, suggesting that the altered molecular rhythms observed in wild-type flies result from the integration of conflicting inputs to the clock network, and that such conflicts can be avoided by weakening one of the input pathways, as in cry02 mutants.

View Article: PubMed Central - PubMed

ABSTRACT

Periodic changes in light and temperature synchronize the Drosophila circadian clock, but the question of how the fly brain integrates these two input pathways to set circadian time remains unanswered. We explore multisensory cue combination by testing the resilience of the circadian network to conflicting environmental inputs. We show that misaligned light and temperature cycles can lead to dramatic changes in the daily locomotor activities of wild-type flies during and after exposure to sensory conflict. This altered behavior is associated with a drastic reduction in the amplitude of PERIOD (PER) oscillations in brain clock neurons and desynchronization between light- and temperature-sensitive neuronal subgroups. The behavioral disruption depends heavily on the phase relationship between light and temperature signals. Our results represent a systematic quantification of multisensory integration in the Drosophila circadian system and lend further support to the view of the clock as a network of coupled oscillatory subunits.

No MeSH data available.


Related in: MedlinePlus