Age-Related Unstructured Spike Patterns and Molecular Localization in Drosophila Circadian Neurons
Aging decreases sleep quality by disrupting the molecular machinery that regulates the circadian rhythm. However, we do not fully understand the mechanism that underlies this process. In Drosophila, sleep quality is regulated by precisely timed patterns of spontaneous firing activity in posterior DN...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-03-01
|
| Series: | Frontiers in Physiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2022.845236/full |
| _version_ | 1818487572965359616 |
|---|---|
| author | Dieu Linh Nguyen Anelise N. Hutson Yutian Zhang Skylar D. Daniels Aidan R. Peard Masashi Tabuchi |
| author_facet | Dieu Linh Nguyen Anelise N. Hutson Yutian Zhang Skylar D. Daniels Aidan R. Peard Masashi Tabuchi |
| author_sort | Dieu Linh Nguyen |
| collection | DOAJ |
| description | Aging decreases sleep quality by disrupting the molecular machinery that regulates the circadian rhythm. However, we do not fully understand the mechanism that underlies this process. In Drosophila, sleep quality is regulated by precisely timed patterns of spontaneous firing activity in posterior DN1 (DN1p) circadian clock neurons. How aging affects the physiological function of DN1p neurons is unknown. In this study, we found that aging altered functional parameters related to neural excitability and disrupted patterned spike sequences in DN1p neurons during nighttime. We also characterized age-associated changes in intrinsic membrane properties related to spike frequency adaptations and synaptic properties, which may account for the unstructured spike patterns in aged DN1p neurons. Because Slowpoke binding protein (SLOB) and the Na+/K+ ATPase β subunit (NaKβ) regulate clock-dependent spiking patterns in circadian networks, we compared the subcellular organization of these factors between young and aged DN1p neurons. Young DN1p neurons showed circadian cycling of HA-tagged SLOB and myc-tagged NaKβ targeting the plasma membrane, whereas aged DN1p neurons showed significantly disrupted subcellular localization patterns of both factors. The distribution of SLOB and NaKβ signals also showed greater variability in young vs. aged DN1p neurons, suggesting aging leads to a loss of actively formed heterogeneity for these factors. These findings showed that aging disrupts precisely structured molecular patterns that regulate structured neural activity in the circadian network, leading to age-associated declines in sleep quality. Thus, it is possible to speculate that a recovery of unstructured neural activity in aging clock neurons could help to rescue age-related poor sleep quality. |
| first_indexed | 2024-12-10T16:39:49Z |
| format | Article |
| id | doaj.art-e6ec33aaaf8f47cea2de28660848d3f2 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-10T16:39:49Z |
| publishDate | 2022-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-e6ec33aaaf8f47cea2de28660848d3f22022-12-22T01:41:16ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-03-011310.3389/fphys.2022.845236845236Age-Related Unstructured Spike Patterns and Molecular Localization in Drosophila Circadian NeuronsDieu Linh NguyenAnelise N. HutsonYutian ZhangSkylar D. DanielsAidan R. PeardMasashi TabuchiAging decreases sleep quality by disrupting the molecular machinery that regulates the circadian rhythm. However, we do not fully understand the mechanism that underlies this process. In Drosophila, sleep quality is regulated by precisely timed patterns of spontaneous firing activity in posterior DN1 (DN1p) circadian clock neurons. How aging affects the physiological function of DN1p neurons is unknown. In this study, we found that aging altered functional parameters related to neural excitability and disrupted patterned spike sequences in DN1p neurons during nighttime. We also characterized age-associated changes in intrinsic membrane properties related to spike frequency adaptations and synaptic properties, which may account for the unstructured spike patterns in aged DN1p neurons. Because Slowpoke binding protein (SLOB) and the Na+/K+ ATPase β subunit (NaKβ) regulate clock-dependent spiking patterns in circadian networks, we compared the subcellular organization of these factors between young and aged DN1p neurons. Young DN1p neurons showed circadian cycling of HA-tagged SLOB and myc-tagged NaKβ targeting the plasma membrane, whereas aged DN1p neurons showed significantly disrupted subcellular localization patterns of both factors. The distribution of SLOB and NaKβ signals also showed greater variability in young vs. aged DN1p neurons, suggesting aging leads to a loss of actively formed heterogeneity for these factors. These findings showed that aging disrupts precisely structured molecular patterns that regulate structured neural activity in the circadian network, leading to age-associated declines in sleep quality. Thus, it is possible to speculate that a recovery of unstructured neural activity in aging clock neurons could help to rescue age-related poor sleep quality.https://www.frontiersin.org/articles/10.3389/fphys.2022.845236/fullDrosophilacircadian clocksleepagingmembrane potentialelectrophysiology |
| spellingShingle | Dieu Linh Nguyen Anelise N. Hutson Yutian Zhang Skylar D. Daniels Aidan R. Peard Masashi Tabuchi Age-Related Unstructured Spike Patterns and Molecular Localization in Drosophila Circadian Neurons Frontiers in Physiology Drosophila circadian clock sleep aging membrane potential electrophysiology |
| title | Age-Related Unstructured Spike Patterns and Molecular Localization in Drosophila Circadian Neurons |
| title_full | Age-Related Unstructured Spike Patterns and Molecular Localization in Drosophila Circadian Neurons |
| title_fullStr | Age-Related Unstructured Spike Patterns and Molecular Localization in Drosophila Circadian Neurons |
| title_full_unstemmed | Age-Related Unstructured Spike Patterns and Molecular Localization in Drosophila Circadian Neurons |
| title_short | Age-Related Unstructured Spike Patterns and Molecular Localization in Drosophila Circadian Neurons |
| title_sort | age related unstructured spike patterns and molecular localization in drosophila circadian neurons |
| topic | Drosophila circadian clock sleep aging membrane potential electrophysiology |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2022.845236/full |
| work_keys_str_mv | AT dieulinhnguyen agerelatedunstructuredspikepatternsandmolecularlocalizationindrosophilacircadianneurons AT anelisenhutson agerelatedunstructuredspikepatternsandmolecularlocalizationindrosophilacircadianneurons AT yutianzhang agerelatedunstructuredspikepatternsandmolecularlocalizationindrosophilacircadianneurons AT skylarddaniels agerelatedunstructuredspikepatternsandmolecularlocalizationindrosophilacircadianneurons AT aidanrpeard agerelatedunstructuredspikepatternsandmolecularlocalizationindrosophilacircadianneurons AT masashitabuchi agerelatedunstructuredspikepatternsandmolecularlocalizationindrosophilacircadianneurons |