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Social facilitation of long-lasting memory is mediated by CO2 in Drosophila.

Aurélie Muria | Pierre-Yves Musso | Matthias Durrieu | Felipe Ramon Portugal | Brice Ronsin | Michael D Gordon | Raphaël Jeanson | Guillaume Isabel
Current biology : CB | 2021

How social interactions influence cognition is a fundamental question, yet rarely addressed at the neurobiological level. It is well established that the presence of conspecifics affects learning and memory performance, but the neural basis of this process has only recently begun to be investigated. In the fruit fly Drosophila melanogaster, the presence of other flies improves retrieval of a long-lasting olfactory memory. Here, we demonstrate that this is a composite memory composed of two distinct elements. One is an individual memory that depends on outputs from the α'β' Kenyon cells (KCs) of the mushroom bodies (MBs), the memory center in the insect brain. The other is a group memory requiring output from the αβ KCs, a distinct sub-part of the MBs. We show that social facilitation of memory increases with group size and is triggered by CO2 released by group members. Among the different known neurons carrying CO2 information in the brain, we establish that the bilateral ventral projection neuron (biVPN), which projects onto the MBs, is necessary for social facilitation. Moreover, we demonstrate that CO2-evoked memory engages a serotoninergic pathway involving the dorsal-paired medial (DPM) neurons, revealing a new role for this pair of serotonergic neurons. Overall, we identified both the sensorial cue and the neural circuit (biVPN>αβ>DPM>αβ) governing social facilitation of memory in flies. This study provides demonstration that being in a group recruits the expression of a cryptic memory and that variations in CO2 concentration can affect cognitive processes in insects.

Pubmed ID: 33740428

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R Project for Statistical Computing (software resource)

RRID:SCR_001905

Software environment and programming language for statistical computing and graphics. R is integrated suite of software facilities for data manipulation, calculation and graphical display. Can be extended via packages. Some packages are supplied with the R distribution and more are available through CRAN family.It compiles and runs on wide variety of UNIX platforms, Windows and MacOS.

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P{VT012760-GAL4}attP2 (organism)

RRID:FlyBase_FBst0484052

Drosophila melanogaster with name P{VT012760-GAL4}attP2 from Flybase.

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P{VT064246-GAL4}attP2 (organism)

RRID:FlyBase_FBst0490696

Drosophila melanogaster with name P{VT064246-GAL4}attP2 from Flybase.

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w[1118]; P{y[+t7.7] w[+mC]=GMR44E04-GAL4}attP2 (organism)

RRID:BDSC_50210

Drosophila melanogaster with name w[1118]; P{y[+t7.7] w[+mC]=GMR44E04-GAL4}attP2 from BDSC.

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w[1118]; P{w[+mW.hs]=GawB}fru[NP0021] (organism)

RRID:BDSC_30027

Drosophila melanogaster with name w[1118]; P{w[+mW.hs]=GawB}fru[NP0021] from BDSC.

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w[1118]; P{y[+t7.7] w[+mC]=GMR53A05-GAL4}attP2 (organism)

RRID:BDSC_38859

Drosophila melanogaster with name w[1118]; P{y[+t7.7] w[+mC]=GMR53A05-GAL4}attP2 from BDSC.

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P{VT048643-GAL4}attP2 (organism)

RRID:FlyBase_FBst0488994

Drosophila melanogaster with name P{VT048643-GAL4}attP2 from Flybase.

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P{VT057244-GAL4}attP2 (organism)

RRID:FlyBase_FBst0489811

Drosophila melanogaster with name P{VT057244-GAL4}attP2 from Flybase.

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y[1] sc[*] v[1] sev[21]; P{y[+t7.7] v[+t1.8]=TRiP.HMS00609}attP2 (organism)

RRID:BDSC_34393

Drosophila melanogaster with name y[1] sc[*] v[1] sev[21]; P{y[+t7.7] v[+t1.8]=TRiP.HMS00609}attP2 from BDSC.

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w[1118]; P{y[+t7.7] w[+mC]=GMR26E07-lexA}attP40 (organism)

RRID:BDSC_52733

Drosophila melanogaster with name w[1118]; P{y[+t7.7] w[+mC]=GMR26E07-lexA}attP40 from BDSC.

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w[1118]; P{w[+mC]=Ddc-GAL4.L}Lmpt[4.36] (organism)

RRID:BDSC_7009

Drosophila melanogaster with name w[1118]; P{w[+mC]=Ddc-GAL4.L}Lmpt[4.36] from BDSC.

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y[1] w[67c23]; P{w[+mW.hs]=GawB}Hr39[c739] (organism)

RRID:BDSC_7362

Drosophila melanogaster with name y[1] w[67c23]; P{w[+mW.hs]=GawB}Hr39[c739] from BDSC.

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National Center for Microscopy and Imaging Research: ImageJ Mosaic Plug-ins (data processing software)

RRID:SCR_001935

THIS RESOURCE IS NO LONGER IN SERVICE. Documented on September 23,2022. 02111-1307, USA. Sponsors: ImageJ Mosaic Plug-Ins software presented here was produced at the National Center for Microscopy and Imaging Research at San Diego, which is supported by the National Institutes of Health (NIH) through a National Center for Research Resources program grant P41 RR04050.

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P{VT030559-GAL4}attP2 (organism)

RRID:FlyBase_FBst0486483

Drosophila melanogaster with name P{VT030559-GAL4}attP2 from Flybase.

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