Modulation of learning safety signals by acute stress: paraventricular thalamus and prefrontal inhibition.
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:
05 Jan 2024
05 Jan 2024
Historique:
received:
16
05
2023
accepted:
18
12
2023
revised:
07
12
2023
medline:
6
1
2024
pubmed:
6
1
2024
entrez:
5
1
2024
Statut:
aheadofprint
Résumé
Distinguishing between cues predicting safety and danger is crucial for survival. Impaired learning of safety cues is a central characteristic of anxiety-related disorders. Despite recent advances in dissecting the neural circuitry underlying the formation and extinction of conditioned fear, the neuronal basis mediating safety learning remains elusive. Here, we showed that safety learning reduces the responses of paraventricular thalamus (PVT) neurons to safety cues, while activation of these neurons controls both the formation and expression of safety memory. Additionally, the PVT preferentially activates prefrontal cortex somatostatin interneurons (SOM-INs), which subsequently inhibit parvalbumin interneurons (PV-INs) to modulate safety memory. Importantly, we demonstrate that acute stress impairs the expression of safety learning, and this impairment can be mitigated when the PVT is inhibited, indicating PVT mediates the stress effect. Altogether, our findings provide insights into the mechanism by which acute stress modulates safety learning.
Identifiants
pubmed: 38182776
doi: 10.1038/s41386-023-01790-2
pii: 10.1038/s41386-023-01790-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Sangha S, Diehl MM, Bergstrom HC, Drew MR. Know safety, no fear. Neurosci Biobehav Rev. 2020;108:218–30.
pubmed: 31738952
doi: 10.1016/j.neubiorev.2019.11.006
Odriozola P, Gee DG. Learning about safety: conditioned inhibition as a novel approach to fear reduction targeting the developing brain. Am J Psychiatry. 2021;178:136–55.
pubmed: 33167673
doi: 10.1176/appi.ajp.2020.20020232
Christianson JP, Fernando AB, Kazama AM, Jovanovic T, Ostroff LE, Sangha S. Inhibition of fear by learned safety signals: a mini-symposium review. J Neurosci. 2012;32:14118–24.
pubmed: 23055481
pmcid: 3541026
doi: 10.1523/JNEUROSCI.3340-12.2012
Jovanovic T, Kazama A, Bachevalier J, Davis M. Impaired safety signal learning may be a biomarker of PTSD. Neuropharmacology. 2012;62:695–704.
pubmed: 21377482
doi: 10.1016/j.neuropharm.2011.02.023
Bouton ME. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol Psychiatry. 2002;52:976–86.
pubmed: 12437938
doi: 10.1016/S0006-3223(02)01546-9
Kida S. Reconsolidation/destabilization, extinction and forgetting of fear memory as therapeutic targets for PTSD. Psychopharmacology. 2019;236:49–57.
pubmed: 30374892
doi: 10.1007/s00213-018-5086-2
Furini C, Myskiw J, Izquierdo I. The learning of fear extinction. Neurosci Biobehav Rev. 2014;47:670–83.
pubmed: 25452113
doi: 10.1016/j.neubiorev.2014.10.016
Tovote P, Fadok JP, Lüthi A. Neuronal circuits for fear and anxiety. Nat Rev Neurosci. 2015;16:317–31.
pubmed: 25991441
doi: 10.1038/nrn3945
Yan R, Wang T, Zhou Q. Elevated dopamine signaling from ventral tegmental area to prefrontal cortical parvalbumin neurons drives conditioned inhibition. Proc Natl Acad Sci USA. 2019;116:13077–86.
pubmed: 31182594
pmcid: 6600914
doi: 10.1073/pnas.1901902116
Sosa R, Ramírez MN. Conditioned inhibition: Historical critiques and controversies in the light of recent advances. J Exp Psychol Anim Learn Cogn. 2019;45:17–42.
pubmed: 30604993
doi: 10.1037/xan0000193
Kong E, Monje FJ, Hirsch J, Pollak DD. Learning not to fear: neural correlates of learned safety. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol. 2014;39:515–27.
doi: 10.1038/npp.2013.191
Rescorla RA. Pavlovian conditioned inhibition. Psychol Bull. 1969;72:77–94.
doi: 10.1037/h0027760
Walasek G, Wesierska M, Zieliński K. Conditioning of fear and conditioning of safety in rats. Acta Neurobiol Exp. 1995;55:121–32.
doi: 10.55782/ane-1995-1067
Tanimoto H, Heisenberg M, Gerber B. Experimental psychology: event timing turns punishment to reward. Nature. 2004;430:983.
pubmed: 15329711
doi: 10.1038/430983a
Paxinos G, Franklin K, Franklin K. The Mouse Brain in Stereotaxic Coordinates, Compact. The Mouse Brain in Stereotaxic Coordinates, Compact.
Do-Monte FH, Quiñones-Laracuente K, Quirk GJ. A temporal shift in the circuits mediating retrieval of fear memory. Nature. 2015;519:460–3.
pubmed: 25600268
pmcid: 4376623
doi: 10.1038/nature14030
Padilla-Coreano N, Do-Monte FH, Quirk GJ. A time-dependent role of midline thalamic nuclei in the retrieval of fear memory. Neuropharmacology. 2012;62:457–63.
pubmed: 21903111
doi: 10.1016/j.neuropharm.2011.08.037
Juruena MF, Eror F, Cleare AJ, Young AH. The role of early life stress in HPA axis and anxiety. Adv Exp Med Biol. 2020;1191:141–53.
pubmed: 32002927
doi: 10.1007/978-981-32-9705-0_9
Bondi CO, Rodriguez G, Gould GG, Frazer A, Morilak DA. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacol : Off Publ Am Coll Neuropsychopharmacol. 2008;33:320–31.
doi: 10.1038/sj.npp.1301410
Wang T, Yan R, Zhang X, Wang Z, Duan H, Wang Z, et al. Paraventricular thalamus dynamically modulates aversive memory via tuning prefrontal inhibitory circuitry. J Neurosci. 2023;43:3630–46.
Barson JR, Mack NR, Gao WJ. The paraventricular nucleus of the thalamus is an important node in the emotional processing network. Front Behav Neurosci. 2020;14:598469.
pubmed: 33192373
pmcid: 7658442
doi: 10.3389/fnbeh.2020.598469
Zhao D, Wang D, Wang W, Dai J, Cui M, Wu M, et al. The altered sensitivity of acute stress induced anxiety-related behaviors by modulating insular cortex-paraventricular thalamus-bed nucleus of the stria terminalis neural circuit. Neurobiol Dis. 2022;174:105890.
pubmed: 36220611
doi: 10.1016/j.nbd.2022.105890
Yan R, Wang T, Ma X, Zhang X, Zheng R, Zhou Q. Prefrontal inhibition drives formation and dynamic expression of probabilistic Pavlovian fear conditioning. Cell Rep. 2021;36:109503.
pubmed: 34380026
doi: 10.1016/j.celrep.2021.109503
Lubow RE. Latent inhibition. Psychol Bull. 1973;79:398–407.
pubmed: 4575029
doi: 10.1037/h0034425
Holt W, Maren S. Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. J Neurosci. 1999;19:9054–62.
pubmed: 10516322
pmcid: 6782751
doi: 10.1523/JNEUROSCI.19-20-09054.1999
Cummings KA, Clem RL. Prefrontal somatostatin interneurons encode fear memory. Nat Neurosci. 2020;23:61–74.
pubmed: 31844314
doi: 10.1038/s41593-019-0552-7
Fadok JP, Krabbe S, Markovic M, Courtin J, Xu C, Massi L, et al. A competitive inhibitory circuit for selection of active and passive fear responses. Nature. 2017;542:96–100.
pubmed: 28117439
doi: 10.1038/nature21047
Krabbe S, Paradiso E, d’Aquin S, Bitterman Y, Courtin J, Xu C, et al. Adaptive disinhibitory gating by VIP interneurons permits associative learning. Nat Neurosci. 2019;22:1834–43.
pubmed: 31636447
doi: 10.1038/s41593-019-0508-y
Roy DS, Park YG, Kim ME, Zhang Y, Ogawa SK, DiNapoli N, et al. Brain-wide mapping reveals that engrams for a single memory are distributed across multiple brain regions. Nat Commun. 2022;13:1799.
pubmed: 35379803
pmcid: 8980018
doi: 10.1038/s41467-022-29384-4
Bubser M, Deutch AY. Stress induces Fos expression in neurons of the thalamic paraventricular nucleus that innervate limbic forebrain sites. Synapse. 1999;32:13–22.
pubmed: 10188633
doi: 10.1002/(SICI)1098-2396(199904)32:1<13::AID-SYN2>3.0.CO;2-R
Gao C, Leng Y, Ma J, Rooke V, Rodriguez-Gonzalez S, Ramakrishnan C, et al. Two genetically, anatomically and functionally distinct cell types segregate across anteroposterior axis of paraventricular thalamus. Nat Neurosci. 2020;23:217–28.
pubmed: 31932767
pmcid: 7007348
doi: 10.1038/s41593-019-0572-3
Otake K, Kin K, Nakamura Y. Fos expression in afferents to the rat midline thalamus following immobilization stress. Neurosci Res. 2002;43:269–82.
pubmed: 12103445
doi: 10.1016/S0168-0102(02)00042-1
Spencer SJ, Fox JC, Day TA. Thalamic paraventricular nucleus lesions facilitate central amygdala neuronal responses to acute psychological stress. Brain Res. 2004;997:234–7.
pubmed: 14706875
doi: 10.1016/j.brainres.2003.10.054
Zhu L, Wu L, Yu B, Liu X. The participation of a neurocircuit from the paraventricular thalamus to amygdala in the depressive like behavior. Neurosci Lett. 2011;488:81–6.
pubmed: 21073922
doi: 10.1016/j.neulet.2010.11.007
Olff M. Sex and gender differences in post-traumatic stress disorder: an update. Eur J Psychotraumatol. 2017;8(sup4):1351204.
Kooiker CL, Birnie MT, Baram TZ. The Paraventricular Thalamus: A potential sensor and integrator of emotionally salient early-life experiences. Front Behav Neurosci. 2021;15:673162.
pubmed: 34079442
pmcid: 8166219
doi: 10.3389/fnbeh.2021.673162
Li S, Kirouac GJ. Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J Comp Neurol. 2008;506:263–87.
pubmed: 18022956
doi: 10.1002/cne.21502
Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci USA. 2005;102:9371–6.
pubmed: 15967994
pmcid: 1166638
doi: 10.1073/pnas.0504011102
Roozendaal B, McEwen BS, Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci. 2009;10:423–33.
pubmed: 19469026
doi: 10.1038/nrn2651
Chauveau F, Lange MD, Jüngling K, Lesting J, Seidenbecher T, Pape HC. Prevention of stress-impaired fear extinction through neuropeptide s action in the lateral amygdala. Neuropsychopharmacology. 2012;37:1588–99.
pubmed: 22298122
pmcid: 3358750
doi: 10.1038/npp.2012.3
Choi EA, Jean-Richard-Dit-Bressel P, Clifford CWG, McNally GP. Paraventricular thalamus controls behavior during motivational conflict. J Neurosci. 2019;39:4945–58.
pubmed: 30979815
pmcid: 6670259
doi: 10.1523/JNEUROSCI.2480-18.2019
Van der Werf YD, Witter MP, Groenewegen HJ. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev. 2002;39:107–40.
pubmed: 12423763
doi: 10.1016/S0165-0173(02)00181-9
Vogt BA, Hof PR, Friedman DP, Sikes RW, Vogt LJ. Norepinephrinergic afferents and cytology of the macaque monkey midline, mediodorsal, and intralaminar thalamic nuclei. Brain Struct Funct. 2008;212:465–79.
pubmed: 18317800
pmcid: 2649766
doi: 10.1007/s00429-008-0178-0
Iglesias AG, Flagel SB. The Paraventricular Thalamus as a critical node of motivated behavior via the hypothalamic-thalamic-striatal circuit. Front Integr Neurosci. 2021;15:706713.
pubmed: 34220458
pmcid: 8250420
doi: 10.3389/fnint.2021.706713
Otis JM, Zhu M, Namboodiri VMK, Cook CA, Kosyk O, Matan AM, et al. Paraventricular Thalamus projection neurons integrate cortical and hypothalamic signals for cue-reward processing. Neuron. 2019;103:423–31.e4.
pubmed: 31196673
pmcid: 6773659
doi: 10.1016/j.neuron.2019.05.018
Campus P, Covelo IR, Kim Y, Parsegian A, Kuhn BN, Lopez SA, et al. The paraventricular thalamus is a critical mediator of top-down control of cue-motivated behavior in rats. Elife. 2019;8:e49041.
Zhu Y, Wienecke CF, Nachtrab G, Chen X. A thalamic input to the nucleus accumbens mediates opiate dependence. Nature. 2016;530:219–22.
pubmed: 26840481
pmcid: 4814115
doi: 10.1038/nature16954
Roozendaal B, Brunson KL, Holloway BL, McGaugh JL, Baram TZ. Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc Natl Acad Sci USA. 2002;99:13908–13.
pubmed: 12361983
pmcid: 129796
doi: 10.1073/pnas.212504599
Rau V, Fanselow MS. Exposure to a stressor produces a long lasting enhancement of fear learning in rats. Stress. 2009;12:125–33.
pubmed: 18609302
doi: 10.1080/10253890802137320
Hermans EJ, Henckens MJ, Joëls M, Fernández G. Dynamic adaptation of large-scale brain networks in response to acute stressors. Trends Neurosci. 2014;37:304–14.
pubmed: 24766931
doi: 10.1016/j.tins.2014.03.006
Gagnon SA, Wagner AD. Acute stress and episodic memory retrieval: neurobiological mechanisms and behavioral consequences. Ann N. Y Acad Sci. 2016;1369:55–75.
pubmed: 26799371
doi: 10.1111/nyas.12996
Packard MG, Goodman J. Emotional arousal and multiple memory systems in the mammalian brain. Front Behav Neurosci. 2012;6:14.
pubmed: 22470324
pmcid: 3313468
doi: 10.3389/fnbeh.2012.00014
Schwabe L. Stress and the engagement of multiple memory systems: integration of animal and human studies. Hippocampus. 2013;23:1035–43.
pubmed: 23929780
doi: 10.1002/hipo.22175
Hamacher-Dang TC, Uengoer M, Wolf OT. Stress impairs retrieval of extinguished and unextinguished associations in a predictive learning task. Neurobiol Learn Mem. 2013;104:1–8.
pubmed: 23623828
doi: 10.1016/j.nlm.2013.04.007
Kinner VL, Wolf OT, Merz CJ. Cortisol increases the return of fear by strengthening amygdala signaling in men. Psychoneuroendocrinology. 2018;91:79–85.
pubmed: 29529523
doi: 10.1016/j.psyneuen.2018.02.020
Merz CJ, Eichholtz A, Wolf OT. Acute stress reduces out-group related safety signaling during fear reinstatement in women. Sci Rep. 2020;10:2092.
pubmed: 32034214
pmcid: 7005737
doi: 10.1038/s41598-020-58977-6
Xu H, Liu L, Tian Y, Wang J, Li J, Zheng J, et al. A disinhibitory microcircuit mediates conditioned social fear in the prefrontal cortex. Neuron. 2019;102:668–82.e5.
pubmed: 30898376
doi: 10.1016/j.neuron.2019.02.026
Courtin J, Chaudun F, Rozeske RR, Karalis N, Gonzalez-Campo C, Wurtz H, et al. Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature. 2014;505:92–6.
pubmed: 24256726
doi: 10.1038/nature12755
Chen YH, Hu NY, Wu DY, Bi LL, Luo ZY, Huang L, et al. PV network plasticity mediated by neuregulin1-ErbB4 signalling controls fear extinction. Mol Psychiatry. 2022;27:896–906.
pubmed: 34697452
doi: 10.1038/s41380-021-01355-z
Pollak DD, Rogan MT, Egner T, Perez DL, Yanagihara TK, Hirsch J. A translational bridge between mouse and human models of learned safety. Ann Med. 2010;42:115–22.
pubmed: 20121549
doi: 10.3109/07853890903583666