Serotonin modulates an inhibitory input to the central amygdala from the ventral periaqueductal gray.
Journal
Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
received:
28
03
2022
accepted:
11
07
2022
revised:
21
06
2022
pubmed:
24
8
2022
medline:
5
11
2022
entrez:
23
8
2022
Statut:
ppublish
Résumé
Fear is an adaptive state that drives defensive behavioral responses to specific and imminent threats. The central nucleus of the amygdala (CeA) is a critical site of adaptations that are required for the acquisition and expression of fear, in part due to alterations in the activity of inputs to the CeA. Here, we characterize a novel GABAergic input to the CeA from the ventral periaqueductal gray (vPAG) using fiber photometry and ex vivo whole-cell slice electrophysiology combined with optogenetics and pharmacology. GABA transmission from this ascending vPAG-CeA input was enhanced by serotonin via activation of serotonin type 2 C (5HT
Identifiants
pubmed: 35999277
doi: 10.1038/s41386-022-01392-4
pii: 10.1038/s41386-022-01392-4
pmc: PMC9630515
doi:
Substances chimiques
Serotonin
333DO1RDJY
valproic acid glucuronide
60113-83-9
gamma-Aminobutyric Acid
56-12-2
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
2194-2204Subventions
Organisme : NIDDK NIH HHS
ID : K01 DK115902
Pays : United States
Organisme : NIAAA NIH HHS
ID : P60 AA011605
Pays : United States
Organisme : NIAAA NIH HHS
ID : F32 AA022549
Pays : United States
Organisme : NIAAA NIH HHS
ID : T32 AA007573
Pays : United States
Organisme : NINDS NIH HHS
ID : T32 NS007431
Pays : United States
Organisme : NIAAA NIH HHS
ID : U01 AA020911
Pays : United States
Informations de copyright
© 2022. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
Références
Herry C, Johansen JP. Encoding of fear learning and memory in distributed neuronal circuits. Nat Neurosci. 2014;17:1644–54.
pubmed: 25413091
doi: 10.1038/nn.3869
Martinez RC, de Oliveira AR, Brandao ML. Conditioned and unconditioned fear organized in the periaqueductal gray are differentially sensitive to injections of muscimol into amygdaloid nuclei. Neurobiol Learn Mem. 2006;85:58–65.
pubmed: 16198609
doi: 10.1016/j.nlm.2005.08.007
Dejean C, Courtin J, Rozeske RR, Bonnet MC, Dousset V, Michelet T, et al. Neuronal Circuits for Fear Expression and Recovery: Recent Advances and Potential Therapeutic Strategies. Biol Psychiatry. 2015;78:298–306.
pubmed: 25908496
doi: 10.1016/j.biopsych.2015.03.017
Tovote P, Fadok JP, Luthi A. Neuronal circuits for fear and anxiety. Nat Rev Neurosci. 2015;16:317–31.
pubmed: 25991441
doi: 10.1038/nrn3945
George DT, Ameli R, Koob GF. Periaqueductal Gray Sheds Light on Dark Areas of Psychopathology. Trends Neurosci. 2019;42:349–60.
pubmed: 30955857
doi: 10.1016/j.tins.2019.03.004
LeDoux JE, Iwata J, Cicchetti P, Reis DJ. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci. 1988;8:2517–29.
pubmed: 2854842
pmcid: 6569498
doi: 10.1523/JNEUROSCI.08-07-02517.1988
Vianna DM, Graeff FG, Landeira-Fernandez J, Brandao ML. Lesion of the ventral periaqueductal gray reduces conditioned fear but does not change freezing induced by stimulation of the dorsal periaqueductal gray. Learn Mem. 2001;8:164–9.
pubmed: 11390636
pmcid: 311373
doi: 10.1101/lm.36101
Zanoveli JM, Carvalho MC, Cunha JM, Brandao ML. Extracellular serotonin level in the basolateral nucleus of the amygdala and dorsal periaqueductal gray under unconditioned and conditioned fear states: an in vivo microdialysis study. Brain Res. 2009;1294:106–15.
pubmed: 19646971
doi: 10.1016/j.brainres.2009.07.074
Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature. 2010;468:277–82.
pubmed: 21068837
doi: 10.1038/nature09559
Kim EJ, Horovitz O, Pellman BA, Tan LM, Li Q, Richter-Levin G, et al. Dorsal periaqueductal gray-amygdala pathway conveys both innate and learned fear responses in rats. Proc Natl Acad. 2013;110:14795–14800.
doi: 10.1073/pnas.1310845110
Haubensak W, Kunwar PS, Cai H, Ciocchi S, Wall NR, Ponnusamy R, et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature. 2010;468:270–6.
pubmed: 21068836
pmcid: 3597095
doi: 10.1038/nature09553
Li H, Penzo MA, Taniguchi H, Kopec CD, Huang ZJ, Li B. Experience-dependent modification of a central amygdala fear circuit. Nat Neurosci. 2013;16:332–9.
pubmed: 23354330
pmcid: 3581751
doi: 10.1038/nn.3322
Penzo MA, Robert V, Li B. Fear conditioning potentiates synaptic transmission onto long-range projection neurons in the lateral subdivision of central amygdala. J Neurosci. 2014;34:2432–7.
pubmed: 24523533
pmcid: 3921418
doi: 10.1523/JNEUROSCI.4166-13.2014
Penzo MA, Robert V, Tucciarone J, De Bundel D, Wang M, Van Aelst L, et al. The paraventricular thalamus controls a central amygdala fear circuit. Nature. 2015;519:455–9.
pubmed: 25600269
pmcid: 4376633
doi: 10.1038/nature13978
Johansen JP, Tarpley JW, LeDoux JE, Blair HT. Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray. Nat Neurosci. 2010;13:979–86.
pubmed: 20601946
pmcid: 2910797
doi: 10.1038/nn.2594
McNally GP, Johansen JP, Blair HT. Placing prediction into the fear circuit. Trends Neurosci. 2011;34:283–92.
pubmed: 21549434
pmcid: 4245078
doi: 10.1016/j.tins.2011.03.005
Roy M, Shohamy D, Daw N, Jepma M, Wimmer GE, Wager TD. Representation of aversive prediction errors in the human periaqueductal gray. Nat Neurosci. 2014;17:1607–12.
pubmed: 25282614
pmcid: 4213247
doi: 10.1038/nn.3832
Rizvi TA, Ennis M, Behbehani MM, Shipley MT. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol. 1991;303:121–31.
pubmed: 1706363
doi: 10.1002/cne.903030111
Bienkowski MS, Rinaman L. Common and distinct neural inputs to the medial central nucleus of the amygdala and anterior ventrolateral bed nucleus of stria terminalis in rats. Brain Struct Funct. 2013;218:187–208.
pubmed: 22362201
doi: 10.1007/s00429-012-0393-6
Fu W, Le Maitre E, Fabre V, Bernard JF, David Xu ZQ, Hokfelt T. Chemical neuroanatomy of the dorsal raphe nucleus and adjacent structures of the mouse brain. J Comp Neurol. 2010;518:3464–94.
pubmed: 20589909
doi: 10.1002/cne.22407
Challis C, Boulden J, Veerakumar A, Espallergues J, Vassoler FM, Pierce RC, et al. Raphe GABAergic neurons mediate the acquisition of avoidance after social defeat. J Neurosci. 2013;33:13978–88, 13988a.
pubmed: 23986235
pmcid: 3756748
doi: 10.1523/JNEUROSCI.2383-13.2013
Lowery-Gionta EG, DiBerto J, Mazzone CM, Kash TL. GABA neurons of the ventral periaqueductal gray area modulate behaviors associated with anxiety and conditioned fear. Brain Struct Funct. 2018;223:3787–99.
pubmed: 30076467
doi: 10.1007/s00429-018-1724-z
Tovote P, Esposito MS, Botta P, Chaudun F, Fadok JP, Markovic M, et al. Midbrain circuits for defensive behaviour. Nature. 2016;534:206–12.
pubmed: 27279213
doi: 10.1038/nature17996
Burghardt NS, Bauer EP. Acute and chronic effects of selective serotonin reuptake inhibitor treatment on fear conditioning: implications for underlying fear circuits. Neuroscience. 2013;247:253–72.
pubmed: 23732229
doi: 10.1016/j.neuroscience.2013.05.050
Marcinkiewcz CA, Mazzone CM, D’Agostino G, Halladay LR, Hardaway JA, DiBerto JF, et al. Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala. Nature. 2016;537:97–101.
pubmed: 27556938
pmcid: 5124365
doi: 10.1038/nature19318
Marcinkiewcz CA, Bierlein-De La Rosa G, Dorrier CE, McKnight M, DiBerto JF, Pati D, et al. Sex-Dependent Modulation of Anxiety and Fear by 5-HT1A Receptors in the Bed Nucleus of the Stria Terminalis. ACS Chem Neurosci. 2019;10:3154–66.
pubmed: 31140276
doi: 10.1021/acschemneuro.8b00594
Unger EK, Keller JP, Altermatt M, Liang R, Matsui A, Dong C, et al. Directed Evolution of a Selective and Sensitive Serotonin Sensor via Machine Learning. Cell. 2020;183:1986–2002.e26.
pubmed: 33333022
pmcid: 8025677
doi: 10.1016/j.cell.2020.11.040
Ren J, Friedmann D, Xiong J, Liu CD, Ferguson BR, Weerakkody T, et al. Anatomically Defined and Functionally Distinct Dorsal Raphe Serotonin Sub-systems. Cell. 2018;175:472–87 e20.
pubmed: 30146164
pmcid: 6173627
doi: 10.1016/j.cell.2018.07.043
Rainnie DG. Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol. 1999;82:69–85.
pubmed: 10400936
doi: 10.1152/jn.1999.82.1.69
Spoida K, Masseck OA, Deneris ES, Herlitze S. Gq/5-HT2c receptor signals activate a local GABAergic inhibitory feedback circuit to modulate serotonergic firing and anxiety in mice. Proc Natl Acad Sci. 2014;111:6479–84.
pubmed: 24733892
pmcid: 4035925
doi: 10.1073/pnas.1321576111
Theile JW, Morikawa H, Gonzales RA, Morrisett RA. Role of 5-hydroxytryptamine2C receptors in Ca2+-dependent ethanol potentiation of GABA release onto ventral tegmental area dopamine neurons. J Pharm Exp Ther. 2009;329:625–33.
doi: 10.1124/jpet.108.147793
Vong L, Ye C, Yang Z, Choi B, Chua S, Lowell BB. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron. 2011;71:142–54.
pubmed: 21745644
pmcid: 3134797
doi: 10.1016/j.neuron.2011.05.028
Mathis A, Mamidanna P, Cury KM, Abe T, Murthy VN, Mathis MW, et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat Neurosci. 2018;21:1281–9.
pubmed: 30127430
doi: 10.1038/s41593-018-0209-y
Nilsson SR, Goodwin NL, Choong JJ, Hwang S, Wright HR, Norville ZC, et al. Simple Behavioral Analysis (SimBA) – an open source toolkit for computer classification of complex social behaviors in experimental animals. 2020. bioRxiv. https://doi.org/10.1101/2020.04.19.049452 .
Martianova E, Aronson S, Proulx CD Multi-Fiber Photometry to Record Neural Activity in Freely-Moving Animals. J Vis Exp JoVE. 2019. 20 October 2019. https://doi.org/10.3791/60278 .
Lowery-Gionta EG, Marcinkiewcz CA, Kash TL. Functional alterations in the dorsal raphe nucleus following acute and chronic ethanol exposure. Neuropsychopharmacology. 2015;40:590–600.
pubmed: 25120075
doi: 10.1038/npp.2014.205
Lowery-Gionta EG, Crowley NA, Bukalo O, Silverstein S, Holmes A, Kash TL. Chronic stress dysregulates amygdalar output to the prefrontal cortex. Neuropharmacology. 2018;139:68–75.
pubmed: 29959957
pmcid: 6067970
doi: 10.1016/j.neuropharm.2018.06.032
Khom S, Wolfe SA, Patel RR, Kirson D, Hedges DM, Varodayan FP, et al. Alcohol Dependence and Withdrawal Impair Serotonergic Regulation of GABA Transmission in the Rat Central Nucleus of the Amygdala. J Neurosci. 2020;40:6842–53.
pubmed: 32769108
pmcid: 7470924
doi: 10.1523/JNEUROSCI.0733-20.2020
Barnes NM, Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology. 1999;38:1083–152.
pubmed: 10462127
doi: 10.1016/S0028-3908(99)00010-6
Nicholson AA, Friston KJ, Zeidman P, Harricharan S, McKinnon MC, Densmore M, et al. Dynamic causal modeling in PTSD and its dissociative subtype: Bottom-up versus top-down processing within fear and emotion regulation circuitry. Hum Brain Mapp. 2017;38:5551–61.
pubmed: 28836726
pmcid: 6866710
doi: 10.1002/hbm.23748
Sengupta A, Holmes A. A Discrete Dorsal Raphe to Basal Amygdala 5-HT Circuit Calibrates Aversive Memory. Neuron. 2019;103:489–505.e7.
pubmed: 31204082
pmcid: 6687558
doi: 10.1016/j.neuron.2019.05.029
Amat J, Matus-Amat P, Watkins LR, Maier SF. Escapable and inescapable stress differentially alter extracellular levels of 5-HT in the basolateral amygdala of the rat. Brain Res. 1998;812:113–20.
pubmed: 9813270
doi: 10.1016/S0006-8993(98)00960-3
Tokunaga R, Shimoju R, Takagi N, Shibata H, Kurosawa M. Serotonin release in the central nucleus of the amygdala in response to noxious and innocuous cutaneous stimulation in anesthetized rats. J Physiol Sci. 2016;66:307–14.
pubmed: 26668011
doi: 10.1007/s12576-015-0426-z
Ren J, Isakova A, Friedmann D, Zeng J, Grutzner SM, Pun A, et al. Single-cell transcriptomes and whole-brain projections of serotonin neurons in the mouse dorsal and median raphe nuclei. ELife. 2019;8:e49424.
pubmed: 31647409
pmcid: 6812963
doi: 10.7554/eLife.49424
Becamel C, Gavarini S, Chanrion B, Alonso G, Galeotti N, Dumuis A, et al. The serotonin 5-HT2A and 5-HT2C receptors interact with specific sets of PDZ proteins. J Biol Chem. 2004;279:20257–66.
pubmed: 14988405
doi: 10.1074/jbc.M312106200
Namburi P, Beyeler A, Yorozu S, Calhoon GG, Halbert SA, Wichmann R, et al. A circuit mechanism for differentiating positive and negative associations. Nature. 2015;520:675–8.
pubmed: 25925480
pmcid: 4418228
doi: 10.1038/nature14366
Duvarci S, Popa D, Pare D. Central amygdala activity during fear conditioning. J Neurosci. 2011;31:289–94.
pubmed: 21209214
pmcid: 3080118
doi: 10.1523/JNEUROSCI.4985-10.2011
Wright KM, McDannald MA. Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output. ELife. 2019;8:e45013.
pubmed: 30843787
pmcid: 6435320
doi: 10.7554/eLife.45013
Wright KM, Jhou TC, Pimpinelli D, McDannald MA. Cue-inhibited ventrolateral periaqueductal gray neurons signal fear output and threat probability in male rats. ELife. 2019;8:e50054.
pubmed: 31566567
pmcid: 6821491
doi: 10.7554/eLife.50054
Gruene TM, Flick K, Stefano A, Shea SD, Shansky RM. Sexually divergent expression of active and passive conditioned fear responses in rats. ELife. 2015;4:e11352.
pubmed: 26568307
pmcid: 4709260
doi: 10.7554/eLife.11352
Sramek JJ, Murphy MF, Cutler NR. Sex differences in the psychopharmacological treatment of depression. Dialogues Clin Neurosci. 2016;18:447–57.
pubmed: 28179816
pmcid: 5286730
doi: 10.31887/DCNS.2016.18.4/ncutler