The neural basis for a persistent internal state in


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
23 11 2020
Historique:
received: 30 05 2020
accepted: 18 11 2020
pubmed: 24 11 2020
medline: 23 3 2021
entrez: 23 11 2020
Statut: epublish

Résumé

Sustained changes in mood or action require persistent changes in neural activity, but it has been difficult to identify the neural circuit mechanisms that underlie persistent activity and contribute to long-lasting changes in behavior. Here, we show that a subset of Doublesex+ pC1 neurons in the Long-term mental states such as arousal and mood variations rely on persistent changes in the activity of certain neural circuits which have been difficult to identify. For instance, in male fruit flies, the activation of a particular circuit containing ‘P1 neurons’ can escalate aggressive and mating behaviors. However, less is known about the neural networks that underlie arousal in female flies. A group of female-specific, ‘pC1 neurons’ similar to P1 neurons could play this role, but it was unclear whether it could drive lasting changes in female fly behavior. To investigate this question, Deutsch et al. stimulated or shut down pC1 circuits in female flies, and then recorded the insects’ interactions with male flies. Stimulation was accomplished using optogenetics, a technique which allows researchers to precisely control the activity of specially modified light-sensitive neurons. Silencing pC1 neurons in female flies diminished their interest in male partners and their suitor’s courtship songs. Activating these neural circuits made the females more receptive to males; it also triggered long-lasting aggressive behaviors not typically observed in virgin females, such as shoving and chasing. Deutsch et al. then identified the brain cells that pC1 neurons connect to, discovering that these neurons are part of an interconnected circuit also formed of aIPg neurons – a population of fly brain cells that shows sex differences and is linked to female aggression. The brains of females were then imaged as pC1 neurons were switched on, revealing a persistent activity which outlasted the activation in circuits containing both pC1 and aIPg neurons. Thus, these results link neural circuit architecture to long lasting changes in neural activity, and ultimately, in behavior. Future experiments can build on these results to determine how this circuit is activated during natural social interactions.

Autres résumés

Type: plain-language-summary (eng)
Long-term mental states such as arousal and mood variations rely on persistent changes in the activity of certain neural circuits which have been difficult to identify. For instance, in male fruit flies, the activation of a particular circuit containing ‘P1 neurons’ can escalate aggressive and mating behaviors. However, less is known about the neural networks that underlie arousal in female flies. A group of female-specific, ‘pC1 neurons’ similar to P1 neurons could play this role, but it was unclear whether it could drive lasting changes in female fly behavior. To investigate this question, Deutsch et al. stimulated or shut down pC1 circuits in female flies, and then recorded the insects’ interactions with male flies. Stimulation was accomplished using optogenetics, a technique which allows researchers to precisely control the activity of specially modified light-sensitive neurons. Silencing pC1 neurons in female flies diminished their interest in male partners and their suitor’s courtship songs. Activating these neural circuits made the females more receptive to males; it also triggered long-lasting aggressive behaviors not typically observed in virgin females, such as shoving and chasing. Deutsch et al. then identified the brain cells that pC1 neurons connect to, discovering that these neurons are part of an interconnected circuit also formed of aIPg neurons – a population of fly brain cells that shows sex differences and is linked to female aggression. The brains of females were then imaged as pC1 neurons were switched on, revealing a persistent activity which outlasted the activation in circuits containing both pC1 and aIPg neurons. Thus, these results link neural circuit architecture to long lasting changes in neural activity, and ultimately, in behavior. Future experiments can build on these results to determine how this circuit is activated during natural social interactions.

Identifiants

pubmed: 33225998
doi: 10.7554/eLife.59502
pii: 59502
pmc: PMC7787663
doi:
pii:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Video-Audio Media

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS104899
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS111580
Pays : United States
Organisme : NIMH NIH HHS
ID : RF1 MH117815
Pays : United States

Informations de copyright

© 2020, Deutsch et al.

Déclaration de conflit d'intérêts

DD, DP, LE, TP, RF, JC, CG, AC, EI, AB, SD, CM, TM, RL, KL, NK, DI, MC, AH, CJ, WS, JW, HS, MM No competing interests declared

Références

Neuron. 2020 Oct 14;108(1):145-163.e10
pubmed: 32916090
Nat Ecol Evol. 2017 Jun;1(6):0154
pubmed: 28580431
J Neurosci. 2014 Feb 26;34(9):3142-60
pubmed: 24573274
Nature. 2021 Jan;589(7843):577-581
pubmed: 33239786
Nat Biotechnol. 2004 Dec;22(12):1567-72
pubmed: 15558047
Neuron. 2015 Mar 18;85(6):1344-58
pubmed: 25754823
Neuron. 2016 Jul 20;91(2):293-311
pubmed: 27373836
Neuron. 2018 Nov 7;100(3):651-668.e8
pubmed: 30244885
Nature. 2014 Mar 13;507(7491):233-7
pubmed: 24598544
Curr Biol. 2009 Jan 13;19(1):R36-47
pubmed: 19138592
BMC Biol. 2013 Jan 31;11:11
pubmed: 23369160
Nat Neurosci. 2010 Apr;13(4):458-66
pubmed: 20305646
Cell. 2018 May 17;173(5):1265-1279.e19
pubmed: 29775595
Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13339-44
pubmed: 8917592
Curr Biol. 2019 Oct 7;29(19):3200-3215.e5
pubmed: 31564492
Neuron. 2011 Feb 10;69(3):509-22
pubmed: 21315261
Elife. 2020 Sep 07;9:
pubmed: 32880371
Neuron. 2016 Jul 6;91(1):168-81
pubmed: 27292538
Genetics. 2018 May;209(1):31-35
pubmed: 29535151
Semin Cell Dev Biol. 2006 Feb;17(1):20-30
pubmed: 16384719
Curr Biol. 2019 Oct 7;29(19):3216-3228.e9
pubmed: 31474539
Curr Biol. 2010 Sep 28;20(18):1589-601
pubmed: 20832311
Neuron. 2008 Sep 11;59(5):759-69
pubmed: 18786359
Nat Neurosci. 2019 Dec;22(12):2040-2049
pubmed: 31768056
PLoS Biol. 2010 May 04;8(5):e1000365
pubmed: 20454565
Nat Rev Neurosci. 2016 Oct 18;17(11):692-704
pubmed: 27752072
Neuron. 2014 Feb 19;81(4):755-65
pubmed: 24559671
Elife. 2020 Apr 14;9:
pubmed: 32286229
Nat Methods. 2014 Mar;11(3):338-46
pubmed: 24509633
Nat Methods. 2021 Jul;18(7):771-774
pubmed: 34168373
Curr Opin Neurobiol. 2016 Jun;38:74-9
pubmed: 27093585
Nat Methods. 2019 Jan;16(1):117-125
pubmed: 30573820
Neuron. 2012 Oct 4;76(1):1-11
pubmed: 23040802
PLoS Comput Biol. 2007 Feb 23;3(2):e35
pubmed: 17319739
Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):17029-17038
pubmed: 31391301
Nat Neurosci. 2007 Apr;10(4):494-504
pubmed: 17369822
Dev Psychopathol. 2005 Summer;17(3):715-34
pubmed: 16262989
Neuron. 2018 Jul 25;99(2):376-388.e6
pubmed: 29983326
Cell. 2018 Jul 26;174(3):730-743.e22
pubmed: 30033368
Curr Opin Neurobiol. 2004 Dec;14(6):675-84
pubmed: 15582368
Nature. 2013 Jul 18;499(7458):295-300
pubmed: 23868258
Nature. 2013 Nov 7;503(7474):78-84
pubmed: 24201281
Elife. 2015 Mar 06;4:
pubmed: 25748136
Nat Methods. 2014 Mar;11(3):325-32
pubmed: 24363022
Curr Biol. 2017 Aug 7;27(15):2389-2396.e4
pubmed: 28756955
Elife. 2015 Dec 29;4:
pubmed: 26714106
Curr Biol. 2016 Sep 26;26(18):2508-2515
pubmed: 27568592
Cell. 2005 Jun 3;121(5):795-807
pubmed: 15935765
Nature. 2020 Mar;579(7797):101-105
pubmed: 32103180
Cold Spring Harb Symp Quant Biol. 2014;79:199-210
pubmed: 25948637
Horm Behav. 2003 Sep;44(3):293-9
pubmed: 14609551
Bioessays. 2012 Jun;34(6):458-65
pubmed: 22396302
Nat Methods. 2014 Jul;11(7):756-62
pubmed: 24859752
Nature. 2020 Oct;586(7831):730-734
pubmed: 32939094
Neuron. 1995 Mar;14(3):477-85
pubmed: 7695894
Cell. 2018 Oct 18;175(3):709-722.e15
pubmed: 30245010
Curr Biol. 2014 Jul 21;24(14):1584-1595
pubmed: 24998527
Elife. 2019 Jan 17;8:
pubmed: 30652683
Physiol Behav. 2004 Apr;81(2):179-209
pubmed: 15159167
Elife. 2016 Nov 15;5:
pubmed: 27855059
Psychol Rev. 2003 Jan;110(1):145-72
pubmed: 12529060
Biol Rev Camb Philos Soc. 2011 May;86(2):341-66
pubmed: 20636474
J Neurosci Methods. 2017 Nov 1;291:83-94
pubmed: 28782629
Neuron. 2015 Sep 23;87(6):1332-1343
pubmed: 26365767
Curr Opin Neurobiol. 2016 Jun;38:18-26
pubmed: 26851712
Elife. 2020 Nov 03;9:
pubmed: 33141021
Cell. 2014 Mar 27;157(1):187-200
pubmed: 24679535
Neuron. 2020 Jan 22;105(2):322-333.e5
pubmed: 31810837
Nature. 2014 May 29;509(7502):627-32
pubmed: 24739975
Physiol Behav. 2000 Nov 1-15;71(3-4):373-81
pubmed: 11150570
Neuron. 2018 Apr 4;98(1):16-30
pubmed: 29621486
Elife. 2015 Sep 21;4:
pubmed: 26390382
J Cell Biol. 2009 Jul 13;186(1):129-45
pubmed: 19596851
PLoS One. 2015 May 08;10(5):e0126445
pubmed: 25955600
Neuron. 2014 Jul 2;83(1):149-63
pubmed: 24991959
Annu Rev Neurosci. 2017 Jul 25;40:603-627
pubmed: 28772102
Neuron. 2019 Nov 6;104(3):544-558.e6
pubmed: 31471123
Neuron. 2008 Oct 23;60(2):215-34
pubmed: 18957215
J Neurogenet. 2002 Oct-Dec;16(4):229-48
pubmed: 12745633
Curr Biol. 2016 Jun 6;26(11):1395-403
pubmed: 27185554
Curr Biol. 2010 Sep 28;20(18):1602-14
pubmed: 20832315
Nat Methods. 2013 Jan;10(1):64-7
pubmed: 23202433
Nat Neurosci. 2021 Jan;24(1):93-104
pubmed: 33230320
Proc Natl Acad Sci U S A. 2004 Aug 17;101(33):12342-7
pubmed: 15302936
Proc Natl Acad Sci U S A. 2012 Jun 19;109(25):10065-70
pubmed: 22645338
Neuron. 1997 Dec;19(6):1163-74
pubmed: 9427241

Auteurs

David Deutsch (D)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Diego Pacheco (D)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Lucas Encarnacion-Rivera (L)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Talmo Pereira (T)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Ramie Fathy (R)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Jan Clemens (J)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Cyrille Girardin (C)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Adam Calhoun (A)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Elise Ireland (E)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Austin Burke (A)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Sven Dorkenwald (S)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.
Department of Computer Science, Princeton University, Princeton, United States.

Claire McKellar (C)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Thomas Macrina (T)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.
Department of Computer Science, Princeton University, Princeton, United States.

Ran Lu (R)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Kisuk Lee (K)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.
Brain & Cognitive Science Department, Massachusetts Institute of Technology, Cambridge, United States.

Nico Kemnitz (N)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Dodam Ih (D)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Manuel Castro (M)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Akhilesh Halageri (A)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Chris Jordan (C)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

William Silversmith (W)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

Jingpeng Wu (J)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

H Sebastian Seung (HS)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.
Department of Computer Science, Princeton University, Princeton, United States.

Mala Murthy (M)

Princeton Neuroscience Institute, Princeton University, Princeton, United States.

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