Intercalated amygdala clusters orchestrate a switch in fear state.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
received:
21
05
2020
accepted:
28
04
2021
pubmed:
28
5
2021
medline:
5
11
2021
entrez:
27
5
2021
Statut:
ppublish
Résumé
Adaptive behaviour necessitates the formation of memories for fearful events, but also that these memories can be extinguished. Effective extinction prevents excessive and persistent reactions to perceived threat, as can occur in anxiety and 'trauma- and stressor-related' disorders
Identifiants
pubmed: 34040259
doi: 10.1038/s41586-021-03593-1
pii: 10.1038/s41586-021-03593-1
pmc: PMC8402941
mid: NIHMS1724754
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
403-407Subventions
Organisme : Intramural NIH HHS
ID : ZIA AA000411
Pays : United States
Références
Craske, M. G. et al. Anxiety disorders. Nat. Rev. Dis. Primers 3, 17024 (2017).
pubmed: 28470168
doi: 10.1038/nrdp.2017.24
Duvarci, S. & Pare, D. Amygdala microcircuits controlling learned fear. Neuron 82, 966–980 (2014).
pubmed: 24908482
pmcid: 4103014
doi: 10.1016/j.neuron.2014.04.042
Milad, M. R. & Quirk, G. J. Fear extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 63, 129–151 (2012).
pubmed: 22129456
pmcid: 4942586
doi: 10.1146/annurev.psych.121208.131631
Orsini, C. A. & Maren, S. Neural and cellular mechanisms of fear and extinction memory formation. Neurosci. Biobehav. Rev. 36, 1773–1802 (2012).
pubmed: 22230704
pmcid: 3345303
doi: 10.1016/j.neubiorev.2011.12.014
Tovote, P., Fadok, J. P. & Lüthi, A. Neuronal circuits for fear and anxiety. Nat. Rev. Neurosci. 16, 317–331 (2015).
pubmed: 25991441
doi: 10.1038/nrn3945
Li, B. Central amygdala cells for learning and expressing aversive emotional memories. Curr. Opin. Behav. Sci. 26, 40–45 (2019).
pubmed: 31011591
doi: 10.1016/j.cobeha.2018.09.012
LeDoux, J. E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155–184 (2000).
pubmed: 10845062
doi: 10.1146/annurev.neuro.23.1.155
Bouton, M. E. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol. Psychiatry 52, 976–986 (2002).
pubmed: 12437938
doi: 10.1016/S0006-3223(02)01546-9
Herry, C. et al. Neuronal circuits of fear extinction. Eur. J. Neurosci. 31, 599–612 (2010).
pubmed: 20384807
doi: 10.1111/j.1460-9568.2010.07101.x
Busti, D. et al. Different fear states engage distinct networks within the intercalated cell clusters of the amygdala. J. Neurosci. 31, 5131–5144 (2011).
pubmed: 21451049
pmcid: 6622967
doi: 10.1523/JNEUROSCI.6100-10.2011
Collins, D. R. & Paré, D. Spontaneous and evoked activity of intercalated amygdala neurons. Eur. J. Neurosci. 11, 3441–3448 (1999).
pubmed: 10564352
doi: 10.1046/j.1460-9568.1999.00763.x
Millhouse, O. E. The intercalated cells of the amygdala. J. Comp. Neurol. 247, 246–271 (1986).
pubmed: 2424941
doi: 10.1002/cne.902470209
Waclaw, R. R., Ehrman, L. A., Pierani, A. & Campbell, K. Developmental origin of the neuronal subtypes that comprise the amygdalar fear circuit in the mouse. J. Neurosci. 30, 6944–6953 (2010).
pubmed: 20484636
pmcid: 2882074
doi: 10.1523/JNEUROSCI.5772-09.2010
Royer, S., Martina, M. & Paré, D. An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J. Neurosci. 19, 10575–10583 (1999).
pubmed: 10575053
pmcid: 6782425
doi: 10.1523/JNEUROSCI.19-23-10575.1999
Amano, T., Unal, C. T. & Paré, D. Synaptic correlates of fear extinction in the amygdala. Nat. Neurosci. 13, 489–494 (2010).
pubmed: 20208529
pmcid: 2847017
doi: 10.1038/nn.2499
Likhtik, E., Popa, D., Apergis-Schoute, J., Fidacaro, G. A. & Paré, D. Amygdala intercalated neurons are required for expression of fear extinction. Nature 454, 642–645 (2008).
pubmed: 18615014
pmcid: 2528060
doi: 10.1038/nature07167
Asede, D., Bosch, D., Lüthi, A., Ferraguti, F. & Ehrlich, I. Sensory inputs to intercalated cells provide fear-learning modulated inhibition to the basolateral amygdala. Neuron 86, 541–554 (2015).
pubmed: 25843406
doi: 10.1016/j.neuron.2015.03.008
Mańko, M., Geracitano, R. & Capogna, M. Functional connectivity of the main intercalated nucleus of the mouse amygdala. J. Physiol. (Lond.) 589, 1911–1925 (2011).
doi: 10.1113/jphysiol.2010.201475
Grewe, B. F. et al. Neural ensemble dynamics underlying a long-term associative memory. Nature 543, 670–675 (2017).
pubmed: 28329757
pmcid: 5378308
doi: 10.1038/nature21682
Luo, R. et al. A dopaminergic switch for fear to safety transitions. Nat. Commun. 9, 2483 (2018).
pubmed: 29950562
pmcid: 6021378
doi: 10.1038/s41467-018-04784-7
Salinas-Hernández, X. I. et al. Dopamine neurons drive fear extinction learning by signaling the omission of expected aversive outcomes. eLife 7, e38818 (2018).
pubmed: 30421719
pmcid: 6257816
doi: 10.7554/eLife.38818
Strobel, C., Marek, R., Gooch, H. M., Sullivan, R. K. P. & Sah, P. Prefrontal and auditory input to intercalated neurons of the amygdala. Cell Rep. 10, 1435–1442 (2015).
pubmed: 25753409
doi: 10.1016/j.celrep.2015.02.008
Herry, C. et al. Switching on and off fear by distinct neuronal circuits. Nature 454, 600–606 (2008).
pubmed: 18615015
doi: 10.1038/nature07166
Paré, D. & Smith, Y. GABAergic projection from the intercalated cell masses of the amygdala to the basal forebrain in cats. J. Comp. Neurol. 344, 33–49 (1994).
pubmed: 7520456
doi: 10.1002/cne.903440104
Tovote, P. et al. Midbrain circuits for defensive behaviour. Nature 534, 206–212 (2016).
pubmed: 27279213
doi: 10.1038/nature17996
Senn, V. et al. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 81, 428–437 (2014).
pubmed: 24462103
doi: 10.1016/j.neuron.2013.11.006
McGarry, L. M. & Carter, A. G. Inhibitory gating of basolateral amygdala inputs to the prefrontal cortex. J. Neurosci. 36, 9391–9406 (2016).
pubmed: 27605614
pmcid: 5013187
doi: 10.1523/JNEUROSCI.0874-16.2016
Arruda-Carvalho, M. & Clem, R. L. Prefrontal-amygdala fear networks come into focus. Front. Syst. Neurosci. 9, 145 (2015).
pubmed: 26578902
pmcid: 4626554
doi: 10.3389/fnsys.2015.00145
Koyama, M. & Pujala, A. Mutual inhibition of lateral inhibition: a network motif for an elementary computation in the brain. Curr. Opin. Neurobiol. 49, 69–74 (2018).
pubmed: 29353136
doi: 10.1016/j.conb.2017.12.019
Machens, C. K., Romo, R. & Brody, C. D. Flexible control of mutual inhibition: a neural model of two-interval discrimination. Science 307, 1121–1124 (2005).
pubmed: 15718474
doi: 10.1126/science.1104171
Felsenberg, J. et al. Integration of parallel opposing memories underlies memory extinction. Cell 175, 709–722.e15 (2018).
pubmed: 30245010
pmcid: 6198041
doi: 10.1016/j.cell.2018.08.021
Solomon, R. L. & Corbit, J. D. An opponent-process theory of motivation. I. Temporal dynamics of affect. Psychol. Rev. 81, 119–145 (1974).
pubmed: 4817611
doi: 10.1037/h0036128
Zhang, X., Kim, J. & Tonegawa, S. Amygdala reward neurons form and store fear extinction memory. Neuron 105, 1077–1093.e7 (2020).
pubmed: 31952856
doi: 10.1016/j.neuron.2019.12.025
Braak, H. & Braak, E. Neuronal types in the basolateral amygdaloid nuclei of man. Brain Res. Bull. 11, 349–365 (1983).
pubmed: 6640364
doi: 10.1016/0361-9230(83)90171-5
Rousso, D. L. et al. Two pairs of ON and OFF retinal ganglion cells are defined by intersectional patterns of transcription factor expression. Cell Rep. 15, 1930–1944 (2016).
pubmed: 27210758
pmcid: 4889540
doi: 10.1016/j.celrep.2016.04.069
Guenthner, C. J., Miyamichi, K., Yang, H. H., Heller, H. C. & Luo, L. Permanent genetic access to transiently active neurons via TRAP: targeted recombination in active populations. Neuron 78, 773–784 (2013).
pubmed: 23764283
pmcid: 3782391
doi: 10.1016/j.neuron.2013.03.025
Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013).
pubmed: 23868258
pmcid: 3777791
doi: 10.1038/nature12354
Vardy, E. et al. A new DREADD facilitates the multiplexed chemogenetic interrogation of behavior. Neuron 86, 936–946 (2015).
pubmed: 25937170
pmcid: 4441592
doi: 10.1016/j.neuron.2015.03.065
Armbruster, B. N., Li, X., Pausch, M. H., Herlitze, S. & Roth, B. L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl Acad. Sci. USA 104, 5163–5168 (2007).
pubmed: 17360345
pmcid: 1829280
doi: 10.1073/pnas.0700293104
Shemesh, O. A. et al. Temporally precise single-cell-resolution optogenetics. Nat. Neurosci. 20, 1796–1806 (2017).
pubmed: 29184208
pmcid: 5726564
doi: 10.1038/s41593-017-0018-8
Dana, H. et al. Sensitive red protein calcium indicators for imaging neural activity. eLife 5, e12727 (2016).
pubmed: 27011354
pmcid: 4846379
doi: 10.7554/eLife.12727
Dana, H. et al. High-performance calcium sensors for imaging activity in neuronal populations and microcompartments. Nat. Methods 16, 649–657 (2019).
pubmed: 31209382
doi: 10.1038/s41592-019-0435-6
Renier, N. et al. iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159, 896–910 (2014).
pubmed: 25417164
doi: 10.1016/j.cell.2014.10.010
Susaki, E. A. et al. Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell 157, 726–739 (2014).
pubmed: 24746791
doi: 10.1016/j.cell.2014.03.042
Claudi, F. et al. Visualizing anatomically registered data with brainrender. eLife 10, e65751 (2020).
doi: 10.7554/eLife.65751
Ghosh, K. K. et al. Miniaturized integration of a fluorescence microscope. Nat. Methods 8, 871–878 (2011).
pubmed: 21909102
pmcid: 3810311
doi: 10.1038/nmeth.1694
Franklin, K. B. J. & Paxinos, G. The Mouse Brain in Stereotaxic Coordinates (Academic, 1997).
Bukalo, O. et al. Prefrontal inputs to the amygdala instruct fear extinction memory formation. Sci. Adv. 1, e1500251 (2015).
pubmed: 26504902
pmcid: 4618669
doi: 10.1126/sciadv.1500251
Petreanu, L., Huber, D., Sobczyk, A. & Svoboda, K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10, 663–668 (2007).
pubmed: 17435752
doi: 10.1038/nn1891
Tanaka, Y., Tanaka, Y., Furuta, T., Yanagawa, Y. & Kaneko, T. The effects of cutting solutions on the viability of GABAergic interneurons in cerebral cortical slices of adult mice. J. Neurosci. Methods 171, 118–125 (2008).
pubmed: 18430473
doi: 10.1016/j.jneumeth.2008.02.021
Ting, J. T., Daigle, T. L., Chen, Q. & Feng, G. Acute brain slice methods for adult and aging animals: application of targeted patch clamp analysis and optogenetics. Methods Mol. Biol. 1183, 221–242 (2014).
pubmed: 25023312
pmcid: 4219416
doi: 10.1007/978-1-4939-1096-0_14
Lerner, T. N. et al. Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits. Cell 162, 635–647 (2015).
pubmed: 26232229
pmcid: 4790813
doi: 10.1016/j.cell.2015.07.014
Gunaydin, L. A. et al. Natural neural projection dynamics underlying social behavior. Cell 157, 1535–1551 (2014).
pubmed: 24949967
pmcid: 4123133
doi: 10.1016/j.cell.2014.05.017
Lopes, G. et al. Bonsai: an event-based framework for processing and controlling data streams. Front. Neuroinform. 9, 7 (2015).
pubmed: 25904861
pmcid: 4389726
doi: 10.3389/fninf.2015.00007
An, B. et al. Amount of fear extinction changes its underlying mechanisms. eLife 6, e25224 (2017).
pubmed: 28671550
pmcid: 5495569
doi: 10.7554/eLife.25224
Baek, J. et al. Neural circuits underlying a psychotherapeutic regimen for fear disorders. Nature 566, 339–343 (2019).
pubmed: 30760920
doi: 10.1038/s41586-019-0931-y
Pnevmatikakis, E. A. & Giovannucci, A. NoRMCorre: an online algorithm for piecewise rigid motion correction of calcium imaging data. J. Neurosci. Methods 291, 83–94 (2017).
pubmed: 28782629
doi: 10.1016/j.jneumeth.2017.07.031
Hagihara, K. M., Murakami, T., Yoshida, T., Tagawa, Y. & Ohki, K. Neuronal activity is not required for the initial formation and maturation of visual selectivity. Nat. Neurosci. 18, 1780–1788 (2015).
pubmed: 26523644
doi: 10.1038/nn.4155
Kerlin, A. M., Andermann, M. L., Berezovskii, V. K. & Reid, R. C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67, 858–871 (2010).
pubmed: 20826316
pmcid: 3327881
doi: 10.1016/j.neuron.2010.08.002
Gründemann, J. et al. Amygdala ensembles encode behavioral states. Science 364, eaav8736 (2019).
pubmed: 31000636
doi: 10.1126/science.aav8736