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Research ArticleResearch Article: New Research, Disorders of the Nervous System

Temporally and Spatially Localized PKA Activity within Learning and Memory Circuitry Regulated by Network Feedback

James C. Sears and Kendal Broadie
eNeuro 17 March 2022, 9 (2) ENEURO.0450-21.2022; DOI: https://doi.org/10.1523/ENEURO.0450-21.2022
James C. Sears
1Department of Biological Sciences, Vanderbilt University and Medical Center, Nashville, TN 37235
2Vanderbilt Brain Institute, Vanderbilt University and Medical Center, Nashville, TN 37235
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Kendal Broadie
1Department of Biological Sciences, Vanderbilt University and Medical Center, Nashville, TN 37235
2Vanderbilt Brain Institute, Vanderbilt University and Medical Center, Nashville, TN 37235
3Department of Cell and Developmental Biology, Vanderbilt University and Medical Center, Nashville, TN 37235
4Department of Pharmacology, Vanderbilt University and Medical Center, Nashville, TN 37235
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  • Figure 1.
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    Figure 1.

    Early life, sex-dependent PKA activity in Mushroom Body circuit regions. A, Schematic of MB lobes and defined MBON fields (dashed outlines) shown in three layers: α’/β’ (left), α/β (middle), and γ lobes (right). B, C, Representative images of MB lobes with OK107-Gal4 driving UAS-PKA-SPARK at 0 dpe (B) and 7 dpe (C). The MBON fields (dashed circles) and arrows delineate the α’1 and β’1 quantified regions. D, E, PKA-SPARK::GFP puncta number in both regions, including α’1 (D) and β’1 (E). Scatter plots show all data points and mean ± SEM. F, G, MB lobes with OK107-Gal4 driving UAS-PKA-SPARK in female (F) and male (G) at 7 dpe. H, I, Quantification of PKA-SPARK puncta in both α’1 (H) and β’1 (I). Sample size >15 fields in all conditions. Statistics show two-tailed t tests with Welch’s correction (H) or Mann–Whitney tests (D, E, I). Significance: ***p < 0.001.

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    Figure 2.

    PKA-SPARK::GFP reporter levels constant across sex and age groups. A, Representative Western blotting comparing PKA-SPARK::GFP protein levels (anti-GFP) from 0 and 7 dpe time points, in both females and males with OK107-Gal4 driving UAS-PKA-SPARK::GFP. The protein loading control is α-Tubulin (α-tub). Probed proteins are indicated on the left and molecular weights on the right. B, PKA-SPARK::GFP protein levels normalized to the α-tub loading control. Scatter plots show all data points and mean ± SEM. Statistics show Brown–Forsythe and Welch ANOVA tests. Sample size: 9, all conditions. Significance: not significant (n.s.; p > 0.05).

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    Figure 3.

    Localized MB lobe PKA activity signaling enabled by FMRP and Rugose. A, Representative images of MB lobes with OK107-Gal4 driving UAS-PKA-SPARK at 7 dpe in control (left) and dfmr150M null (right). Arrows point to α’1 and β’1 (Fig. 1A). PKA-SPARK::GFP puncta number in α’1 (B) and β’1 (C) regions. D, Similar confocal imaging comparison at 7 dpe in control (left) and rgFDD null (right). E, F, Quantification of PKA-SPARK::GFP puncta number in α’1 (E) and β’1 (F) regions. Note that this comparison is done in males only owing to the X chromosome location of the rugose gene. Scatter plots show all data points and mean ± SEM. Sample size >12 fields in all conditions. Statistics show two-tailed t tests with Welch’s correction (B, C, F) or Mann–Whitney tests (E). Significance: ***p < 0.001.

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    Figure 4.

    Localized circuit PKA activity increased with Meng-Po OE. A–F, Representative images of MB lobes with OK107-Gal4 driving UAS-PKA-SPARK at 0 and 7 dpe in control (A) and with targeted OE of UAS-dFMRP (B), UAS-hFMRP (C), UAS-ΔRGG-hFMRP (D), UAS-Rugose (Rg, E), and UAS-Meng-Po (MP, F). Arrows indicate the α’1 and β’1 regions (Fig. 1A) of normally heightened PKA activity. Arrowhead (F) points to the expanded PKA activity within the γ3 region. G, H, Quantification of PKA-SPARK::GFP puncta in α’1 (G) and β’1 (H) regions. Scatter plots show all data points and mean ± SEM. Sample size: >7 fields in every genotype and at every time point. Statistics show two-tailed t tests with Welch’s correction and Mann–Whitney tests (see statistical table; Table 1). Significance: ***p < 0.001.

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    Figure 5.

    Localized MB lobe PKA activity signaling requires the Meng-Po kinase. A, Representative MB lobe images with OK107-Gal4 driving UAS-PKA-SPARK at both 0 dpe (left) and 7 dpe (right) in the genetic control background. Quantified MBON fields (dashed circles, left) and arrows indicate α’1 and β’1 regions. B, Representative MB lobes images with meng-po RNAi under the same conditions as in A. Scale bar: 10 μm. C, D, Quantification of PKA-SPARK::GFP puncta in α’1 (C) and β’1 (D) MBON fields. Scatter plots show all data points and mean ± SEM. Statistics show Kruskal–Wallis tests. Sample size: >9, all conditions. Significance: ***p < 0.001, not significant (n.s.; p > 0.05).

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    Figure 6.

    Conditional shibirets neurotransmission block increases PKA activity. A–D, Representative images of MB lobes with OK107-Gal4 driving UAS-shibirets at the 0 and 7 dpe time points at the indicated adult rearing temperatures. Dotted outlines define additional MBON regions of elevated PKA activity detected with the PKA-SPARK reporter, and arrowheads indicate expanded α/α’ neuropils. E–H, Quantified number of PKA-SPARK:GFP puncta in defined MB lobe regions. Scatter plots show all data points and the mean ± SEM. Sample size >12 fields in every temperature condition. Statistics show Brown–Forsythe and Welch ANOVA tests (E, G) and Kruskal–Wallis tests (F, H). Significance: *p < 0.05, ***p < 0.001 and not significant (n.s.; p > 0.05).

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    Figure 7.

    MB circuit PKA activity dramatically expanded by synaptic output block. A, B, MB lobes with OK107-Gal4 driving UAS-tetanus toxin light chain (TNT) at both 0 dpe (A) and 7 dpe (B). Arrows indicate expanded PKA activity regions detected with the PKA-SPARK reporter and dotted outlines indicate newly-recruited MBON regions. C–I, Quantification of PKA-SPARK::GFP puncta number in each defined MBON region, including α’1 (C), β’1 (D), γ1 (E), α’3 (F), α3 (G), β’2m (H), and β2 (I). Scatter plots show all data points and the mean ± SEM. Sample size >19 fields in every paired comparison. Statistics show Mann–Whitney tests. Significance: ***p < 0.001.

Tables

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    Table 1

    Statistical tests used to analyze data

    Circuit
    location
    ComparisonData
    structure
    TestSample size
    (# KC fields or
    Western lysates)
    MeanStatisticsp value
    α’10 dpe; 7 dpeNot normalMann–Whitney test38; 340.1; 32.5U = 0p < 0.0001
    β’10 dpe; 7 dpeNot normalMann–Whitney test37; 380.1; 66.8U = 0p < 0.0001
    α’1Female 7 dpe; male 7 dpenormalUnpaired two-tailed t test18; 1650.1; 26.9t = 6.51 df = 26.96p < 0.0001
    β’1Female 7 dpe; male 7 dpeNot normalMann–Whitney test18; 1683.2; 64.5U = 31p < 0.0001
    N/AFemale 0 dpe; male 0 dpeNormalBrown–Forsythe, Welch ANOVA test9; 91.0; 1.104t = 2.028 DF = 15.75p = 0.2846
    N/AFemale 0 dpe; female 7 dpeNormalBrown–Forsythe, Welch ANOVA test9; 91.0; 1.088t = 0.8219 DF = 10.31p = 0.9482
    N/AFemale 0 dpe; male 7 dpeNormalBrown–Forsythe, Welch ANOVA test9; 91.0; 0.9298t = 0.7746 DF = 11.32p = 0.9608
    N/AMale 0 dpe; female 7 dpeNormalBrown–Forsythe, Welch ANOVA test9; 91.104; 1.088t = 0.1493 DF = 9.809p > 0.9999
    N/AMale 0 dpe; male 7 dpeNormalBrown–Forsythe, Welch ANOVA test9; 91.104; 0.9298t = 1.956 DF = 10.63p = 0.3383
    N/AFemale 7 dpe; male 7 dpeNormalBrown–Forsythe, Welch ANOVA test9; 91.088; 0.9298t = 1.223 DF = 15.43p = 0.7724
    α’1Control 7dpe; dfmr1 7dpeNormalUnpaired two-tailed t test34; 2143.5; 26.1t = 3.77 df = 41.34p = 0.0005
    β’1Control 7dpe; dfmr1 7dpeNormalUnpaired two-tailed t test34; 2175.5; 43.9t = 3.88 df = 34.73p = 0.0004
    α’1Control 7dpe; rg 7 dpeNot normalMann–Whitney test24; 1827.4; 15.2U = 70.50p = 0.0001
    β’1Control 7dpe; rg 7 dpeNormalUnpaired two-tailed t test24; 1858.9; 20.8t = 8.40 df = 31.59p < 0.0001
    α’1Control 0 dpe; control 7 dpeNot normalMann–Whitney test14; 120.1; 35.7U = 0p < 0.0001
    α’1dFMRP OE 0 dpe; dFMRP OE 7 dpeNot normalMann–Whitney test16; 185.2; 31.6U = 11.50p < 0.0001
    α’1hFMRP OE 0 dpe; hFMRP OE 7 dpeNot normalMann–Whitney test18; 110.2; 39.8U = 0p < 0.0001
    α’1ΔRGG-hFMRP OE 0 dpe; ΔRGG-hFMRP OE 7 dpeNot normalMann–Whitney test8; 180.1; 5.3U = 9.50p = 0.0001
    α’1Rg OE 0 dpe; Rg OE 7 dpeNormalUnpaired two-tailed t test14; 160.3; 31.6t = 8.94 df = 15.04p < 0.0001
    α’1Meng-Po OE 0 dpe; Meng-Po OE 7dpeNormalUnpaired two-tailed t test16; 1667.1; 196.4t = 7.88 df = 16.78p < 0.0001
    α’1Control 0 dpe; dFMRP OE 0 dpeNot normalKruskal–Wallis test14; 160.1; 5.2Mean rank diff = −22.9p = 0.0272
    α’1Control 0 dpe; hFMRP OE 0 dpeNot normalKruskal–Wallis test14; 180.1; 0.2Mean rank diff = −0.7143p > 0.9999
    α’1Control 0 dpe; ΔRGG-hFMRP OE 0 dpeNot normalKruskal–Wallis test14; 80.1; 0.1Mean rank diff = 0.5357p > 0.9999
    α’1Control 0 dpe; Rg OE 0 dpeNot normalKruskal–Wallis test14; 140.1; 0.3Mean rank diff = −4.286p > 0.9999
    α’1Control 0 dpe; Meng-Po OE 0 dpeNot normalKruskal–Wallis test14; 160.1; 67.1Mean rank diff = −49.21p < 0.0001
    α’1Control 7 dpe; dFMRP OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1835.7; 31.6t = 0.74 DF = 23.56p = 0.9505
    α’1Control 7 dpe; hFMRP OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1135.7; 39.8t = 0.62 DF = 20.17p = 0.9751
    α’1Control 7 dpe; ΔRGG-hFMRP OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1835.7; 5.3t = 6.81 DF = 12.48p < 0.0001
    α’1Control 7 dpe; Rg OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1635.7; 31.6t = 0.74 DF = 22.91p = 0.9508
    α’1Control 7 dpe; Meng-Po OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1635.7;196.4t = 9.74 DF = 17.16p < 0.0001
    β’1Control 0 dpe; control 7 dpeNot normalMann–Whitney test14; 120.1; 53.6U = 0p < 0.0001
    β’1dFMRP OE 0 dpe; dFMRP OE 7 dpeNot normalMann–Whitney test16; 183.4; 19.6U = 48.50p = 0.0005
    β’1hFMRP OE 0 dpe; hFMRP OE 7 dpeNot normalMann–Whitney test18; 111.0; 60.5U = 1p < 0.0001
    β’1ΔRGG-hFMRP OE 0 dpe; ΔRGG-hFMRP OE 7 dpeNot normalMann–Whitney test8; 180.1; 7.1U = 0p < 0.0001
    β’1Rg OE 0 dpe; Rg OE 7 dpeNormalUnpaired two-tailed t test14; 160.4; 25.7t = 9.12 df = 15.12p < 0.0001
    β’1Meng-Po OE 0 dpe; Meng-Po OE 7dpeNormalUnpaired two-tailed t test16; 22138.9; 251.9t = 7.49 df = 26.44p < 0.0001
    β’1Control 0 dpe; dFMRP OE 0 dpeNot normalKruskal–Wallis test14; 160.1; 3.4Mean rank diff = −18.48p = 0.1195
    β’1Control 0 dpe; hFMRP OE 0 dpeNot normalKruskal–Wallis test14; 180.1; 1.0Mean rank diff = −6.127p > 0.9999
    β’1Control 0 dpe; ΔRGG-hFMRP OE 0 dpeNot normalKruskal–Wallis test14; 80.1; 0.1Mean rank diff = −1.634p > 0.9999
    β’1Control 0 dpe; Rg OE 0 dpeNot normalKruskal–Wallis test14; 140.1; 0.4Mean rank diff = −9.179p > 0.9999
    β’1Control 0 dpe; Meng-Po OE 0 dpeNot normalKruskal–Wallis test14; 160.1; 138.9Mean rank diff = −50.82p < 0.0001
    β’1Control 7 dpe; dFMRP OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1853.6; 19.6t = 5.13 DF = 20.78p = 0.0002
    β’1Control 7 dpe; hFMRP OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1153.6; 60.5t = 0.76 DF = 19.17p = 0.9426
    β’1Control 7 dpe; ΔRGG-hFMRP OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1853.6; 7.1t = 8.31 DF = 12.07p < 0.0001
    β’1Control 7 dpe; Rg OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 1653.6; 25.7t = 4.55 DF = 16.56p = 0.0014
    β’1Control 7 dpe; Meng-Po OE 7 dpeNormalBrown–Forsythe, Welch ANOVA test12; 2253.6; 251.9t = 13.07 DF = 26.60p <0.0001
    γ3Control 0 dpe; Meng-Po OE 0 dpeNot normalMann–Whitney test14; 160.0; 99.3U = 14p <0.0001
    γ3Control 7 dpe; Meng-Po OE 7 dpeNot normalMann–Whitney test12; 160.4; 291.8U = 0p <0.0001
    α’1Control 0 dpe; meng-po RNAi 0 dpeNot normalKruskal–Wallis test10; 131.0; 0.5Mean rank diff = 2.212p > 0.9999
    α’1Control 0 dpe; control 7 dpeNot normalKruskal–Wallis test10; 171.0; 31.7Mean rank diff = −24.75p = 0.0004
    α’1Control 0 dpe; meng-po RNAi 7 dpeNot normalKruskal–Wallis test10 ; 161.0; 0.3Mean rank diff = 6.125p > 0.9999
    α’1meng-po RNAi 0 dpe; control 7 dpeNot normalKruskal–Wallis test13; 170.5; 31.7Mean rank diff = −26.96p < 0.0001
    α’1meng-po RNAi 0 dpe; meng-po RNAi 7 dpeNot normalKruskal–Wallis test13; 160.5; 0.3Mean rank diff = 3.913p > 0.9999
    α’1Control 7 dpe; meng-po RNAi 7 dpeNot normalKruskal–Wallis test17; 1631.7; 0.3Mean rank diff = 30.88p < 0.0001
    β’1Control 0 dpe; meng-po RNAi 0 dpeNot normalKruskal–Wallis test10; 130.8; 0.3Mean rank diff = 7.138p > 0.9999
    β’1Control 0 dpe; control 7 dpeNot normalKruskal–Wallis test10; 170.8; 41.7Mean rank diff = −23.90p = 0.0007
    β’1Control 0 dpe; meng-po RNAi 7 dpeNot normalKruskal–Wallis test10 ; 160.8; 0.6Mean rank diff = 4.194p > 0.9999
    β’1meng-po RNAi 0 dpe; control 7 dpeNot normalKruskal–Wallis test13; 170.3; 41.7Mean rank diff = −31.04p < 0.0001
    β’1meng-po RNAi 0 dpe; meng-po RNAi 7 dpeNot normalKruskal–Wallis test13; 160.3; 0.6Mean rank diff = −2.945p > 0.9999
    β’1Control 7 dpe; meng-po RNAi 7 dpeNot normalKruskal–Wallis test17; 1641.7; 0.6Mean rank diff = 28.09p < 0.0001
    α’1shibirets 7 dpe 20°C; 25°CNormalBrown–Forsythe, Welch ANOVA test15; 147.5; 25.5t = 3.74 DF = 16.00p = 0.0053
    α’1shibirets 7 dpe 20°C; 33°CNormalBrown–Forsythe, Welch ANOVA test15; 177.5; 62.2t = 11.90 DF =20.01p < 0.0001
    α’1shibirets 7 dpe 25°C; 33°CNormalBrown–Forsythe, Welch ANOVA test14; 1725.5; 62.2t = 5.844 DF = 28.31p < 0.0001
    β’1shibirets 7 dpe 20°C; 25°CNot normalKruskal–Wallis test16; 1418.8; 25.6Mean rank diff = −3.808p > 0.9999
    β’1shibirets 7 dpe 20°C; 33°CNot normalKruskal–Wallis test16; 1718.8; 66.9Mean rank diff = −24.08p < 0.0001
    β’1shibirets 7 dpe 25°C; 33°CNot normalKruskal–Wallis test14; 1725.6; 66.9Mean rank diff = −20.27p = 0.0001
    α2shibirets 7 dpe 20°C; 25°CNormalBrown–Forsythe, Welch ANOVA test16; 1311.1; 53.8t = 9.33 DF = 16.03p <0.0001
    α2shibirets 7 dpe 20°C; 33°CNormalBrown–Forsythe, Welch ANOVA test16; 1711.1; 9.3t = 0.67 DF = 30.76p = 0.8747
    α2shibirets 7 dpe 25°C; 33°CNormalBrown–Forsythe, Welch ANOVA test13; 1753.8; 9.3t = 9.53 DF = 17.13p < 0.0001
    γ1shibirets 7 dpe 20°C; 25°CNot normalKruskal–Wallis test16; 141.9; 0.9Mean rank diff = 4.353p > 0.9999
    γ1shibirets 7 dpe 20°C; 33°CNot normalKruskal–Wallis test16; 171.9; 101.8Mean rank diff = −21.47p < 0.0001
    γ1shibirets 7 dpe 25°C; 33°CNot normalKruskal–Wallis test14; 170.9; 101.8Mean rank diff = −25.82p < 0.0001
    α2shibirets 7 dpe 20°C; 7 dpe 20°C, 3 h 33°CNot normalMann–Whitney test30; 263.6; 26.6U = 82.50p <0.0001
    α’1UAS-TNT 0 dpe; UAS-TNT 7 dpeNot normalMann–Whitney test32; 571.2; 72.4U = 0p <0.0001
    β’1UAS-TNT 0 dpe; UAS-TNT 7 dpeNot normalMann–Whitney test32; 570.5; 75.2U = 3.50p < 0.0001
    γ1UAS-TNT 0 dpe; UAS-TNT 7 dpeNot normalMann–Whitney test31; 570.6; 18.5U = 165.50p < 0.0001
    α'3UAS-TNT 0 dpe; UAS-TNT 7 dpeNot normalMann–Whitney test29; 540.3; 30.1U = 154p < 0.0001
    α3UAS-TNT 0 dpe; UAS-TNT 7 dpeNot normalMann–Whitney test20; 490.2; 66.8U = 0p < 0.0001
    β’2mUAS-TNT 0 dpe; UAS-TNT 7 dpeNot normalMann–Whitney test31; 570.6; 44.1U = 0p < 0.0001
    β2UAS-TNT 0 dpe; UAS-TNT 7 dpeNot normalMann–Whitney test32; 580.2; 85.1U = 0p < 0.0001
    α’1Control; UAS-TNT 7 dpeNot normalMann–Whitney test68; 5735.9; 72.4U = 451.50p < 0.0001
    β’1Control; UAS-TNT 7 dpeNormalUnpaired two-tailed t test72; 5770.4; 75.2t = 0.83 df = 75.77p = 0.41
    α’1 and
    β’1
    α’1 UAS-TNT 7 dpe; β’1 UAS-TNT 7 dpeNormalUnpaired two-tailed t test57; 5772.4; 75.2t =0.43 df = 101.59p = 0.67
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Temporally and Spatially Localized PKA Activity within Learning and Memory Circuitry Regulated by Network Feedback
James C. Sears, Kendal Broadie
eNeuro 17 March 2022, 9 (2) ENEURO.0450-21.2022; DOI: 10.1523/ENEURO.0450-21.2022

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Temporally and Spatially Localized PKA Activity within Learning and Memory Circuitry Regulated by Network Feedback
James C. Sears, Kendal Broadie
eNeuro 17 March 2022, 9 (2) ENEURO.0450-21.2022; DOI: 10.1523/ENEURO.0450-21.2022
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Keywords

  • Drosophila
  • FMRP
  • Kenyon cell
  • Meng-Po
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  • neurobeachin

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Copyright © 2023 by the Society for Neuroscience.
eNeuro eISSN: 2373-2822

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