Amygdala-Prefrontal Synchronization Underlies Resistance to Extinction of Aversive Memories
Open accessAbstract
Emotional memories can persist for a lifetime but can also undergo extinction. Although we know about the mechanisms involved in expression and extinction, we know very little about the mechanisms that determine whether a specific memory would persist or not. Here, we use partial reinforcement extinction effect (PREE) to explore the neural mechanisms that differentiate persistent from labile memories. We recorded the simultaneous activity of neurons in the amygdala and the dorsal anterior cingulate cortex (dACC) while monkeys engaged in tone-odor aversive conditioning. We report that under continuous reinforcement schedule (ConS), activity in the amygdala precedes behavioral response, whereas under partial schedule (ParS), dACC activity precedes it. Moreover, we find that ParS induced cross-regional pairwise correlations throughout the entire acquisition session, and their magnitude and precision predicted the later resistance to extinction. Our results suggest that memory persistence depends on distributed representations and, specifically, resistance to extinction of aversive memories is maintained by correlated amygdala-dACC activity.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Correlated activity between the dorsal anterior cingulate region of the PFC and BLA underlies acquisition of aversive memories.
“Correlated activity between the dorsal anterior cingulate region of the PFC and BLA underlies acquisition of aversive memories”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [104]
Maintenance of cross-regional correlations between the dorsal anterior cingulate region of the PFC and BLA promotes resistance to extinction of fear memories.
“maintenance of such cross-regional correlations promotes resistance to extinction of fear memories104.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [104]
Cites
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Anterior Cingulate Cortex, Error Detection, and the Online Monitoring of Performance
Carter, C. S., Braver, T. S., Barch, D. M., Botvinick, M. M., Noll, D., & Cohen, J. D. (1998) · Science · doi:10.1126/science.280.5364.747 · Cited by 3,273 · see citing works
THE AMYGDALA MODULATES THE CONSOLIDATION OF MEMORIES OF EMOTIONALLY AROUSING EXPERIENCES
McGaugh, J. L. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144157 · Cited by 2,296 · see citing works
Context, time, and memory retrieval in the interference paradigms of Pavlovian learning
Bouton, M. E. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.1.80 · Cited by 1,896 · see citing works
Neurons in medial prefrontal cortex signal memory for fear extinction
Milad, M. R., & Quirk, G. J. (2002) · Nature · doi:10.1038/nature01138 · Cited by 1,836 · cited 1× · see citing works
“This includes the rodent infralimbic cortex (IL) (Milad and Quirk, 2002; Sierra-Mercado et al., 2011) and the primate vmPFC (Phelps et al.”
Phelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.042 · Cited by 1,753 · see citing works
Fear Extinction as a Model for Translational Neuroscience: Ten Years of Progress
Milad, M. R., & Quirk, G. J. (2012) · Annual Review of Psychology · doi:10.1146/annurev.psych.121208.131631 · Cited by 1,466 · see citing works
Neurobiological Basis of Failure to Recall Extinction Memory in Posttraumatic Stress Disorder
Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., Zeidan, M. A., Handwerger, K., Orr, S. P., & Rauch, S. L. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.026 · Cited by 1,339 · see citing works
Cortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303 · see citing works
Myers, K. M., & Davis, M. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001939 · Cited by 1,277 · see citing works
Baxter, M. G., & Murray, E. A. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn875 · Cited by 1,200 · see citing works
Sierra-Mercado, D., Padilla-Coreano, N., & Quirk, G. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.184 · Cited by 1,190 · see citing works
Dynamics of neuronal firing correlation: modulation of "effective connectivity"
Aertsen, A. M. H. J., Gerstein, G. L., Habib, M., & Palm, G. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.5.900 · Cited by 1,073 · see citing works
Medial prefrontal cortex as an action-outcome predictor
Alexander, W. H., & Brown, J. W. (2011) · Nature Neuroscience · doi:10.1038/nn.2921 · Cited by 1,000 · see citing works
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
Switching on and off fear by distinct neuronal circuits
Herry, C., Ciocchi, S., Senn, V., Demmou, L., Müller, C., & Lüthi, A. (2008) · Nature · doi:10.1038/nature07166 · Cited by 950 · see citing works
Encoding of conditioned fear in central amygdala inhibitory circuits
Ciocchi, S., Herry, C., Grenier, F., Wolff, S. B. E., Letzkus, J. J., Vlachos, I., Ehrlich, I., Sprengel, R., Deisseroth, K., Stadler, M. B., et al. (2010) · Nature · doi:10.1038/nature09559 · Cited by 924 · see citing works
Amygdala activity related to enhanced memory for pleasant and aversive stimuli
Hamann, S. B., Ely, T. D., Grafton, S. T., & Kilts, C. D. (1999) · Nature Neuroscience · doi:10.1038/6404 · Cited by 913 · see citing works
Choice, uncertainty and value in prefrontal and cingulate cortex
Rushworth, M. F. S., & Behrens, T. E. J. (2008) · Nature Neuroscience · doi:10.1038/nn2066 · Cited by 866 · see citing works
Ghashghaei, H. T., Hilgetag, C. C., & Barbas, H. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.046 · Cited by 845 · see citing works
New Vistas on Amygdala Networks in Conditioned Fear
Paré, D., Quirk, G. J., & Ledoux, J. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00153.2004 · Cited by 841 · cited 1× · see citing works
“Direct sensory inputs that converge on single cells in the amygdala and induce synaptic plasticity have been directly related to acquisition of fear (Herry et al., 2008; Pape and Pare, 2010; Paré et al., 2004), and the rich repertoire of inputs to the primate amygdala suggests that it is highly adapted for rapid detec…”
Adhikari, A., Topiwala, M. A., & Gordon, J. A. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.002 · Cited by 729 · see citing works
Vidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S. L., & Quirk, G. J. (2006) · Learning & Memory · doi:10.1101/lm.306106 · Cited by 705 · see citing works
Fear extinction in rats: Implications for human brain imaging and anxiety disorders
Milad, M. R., Rauch, S. L., Pitman, R. K., & Quirk, G. J. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.008 · Cited by 597 · cited 1× · see citing works
“Impaired fear extinction leads to maladaptive and persistent expression of fear in the absence of actual threat and is hypothesized to underlie various mood and anxiety disorders (Delgado et al., 2006; Milad et al., 2006; Myers and Davis, 2007).”
Burgos-Robles, A., Vidal-Gonzalez, I., & Quirk, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-09.2009 · Cited by 530 · see citing works
A Role for the Human Dorsal Anterior Cingulate Cortex in Fear Expression
Milad, M. R., Quirk, G. J., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.032 · Cited by 485 · see citing works
Neuronal circuits of fear extinction
Herry, C., Ferraguti, F., Singewald, N., Letzkus, J. J., Ehrlich, I., & Lüthi, A. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07101.x · Cited by 484 · see citing works
Induction of Fear Extinction with Hippocampal-Infralimbic BDNF
Peters, J., Dieppa-Perea, L. M., Melendez, L. M., & Quirk, G. J. (2010) · Science · doi:10.1126/science.1186909 · Cited by 462 · see citing works
Amygdala–frontal interactions and reward expectancy
Holland, P. C., & Gallagher, M. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.007 · Cited by 390 · see citing works
Hayden, B. Y., Heilbronner, S. R., Pearson, J. M., & Platt, M. L. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4652-10.2011 · Cited by 379 · see citing works
Extending animal models of fear conditioning to humans
Delgado, M. R., Olsson, A., & Phelps, E. A. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.006 · Cited by 366 · see citing works
Differential roles of human striatum and amygdala in associative learning
Li, J., Schiller, D., Schoenbaum, G. M., Phelps, E. A., & Daw, N. D. (2011) · Nature Neuroscience · doi:10.1038/nn.2904 · Cited by 364 · see citing works
Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala
Belova, M. A., Paton, J. J., Morrison, S. E., & Salzman, C. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.004 · Cited by 349 · see citing works
Some observations on cortical inputs to the macaque monkey amygdala: An anterograde tracing study
Stefanacci, L., & Amaral, D. G. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10339 · Cited by 345 · see citing works
Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep
Popa, D., Duvarci, S., Popescu, A. T., Léna, C., & Paré, D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913016107 · Cited by 338 · see citing works
Lesting, J., Narayanan, R. T., Kluge, C., Sangha, S., Seidenbecher, T., & Pape, H.-C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021714 · Cited by 275 · see citing works
Central Amygdala Activity during Fear Conditioning
Duvarci, S., Popa, D., & Paré, D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4985-10.2011 · Cited by 202 · see citing works
Herry, C., & Mons, N. E. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03542.x · Cited by 192 · see citing works
Heterogeneous reward signals in prefrontal cortex
Wallis, J. D., & Kennerley, S. W. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.009 · Cited by 186 · see citing works
Basolateral amygdala is not critical for cognitive memory of contextual fear conditioning
Vazdarjanova, A., & McGaugh, J. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.15003 · Cited by 176 · see citing works
Shin, L. M., Bush, G., Milad, M. R., Lasko, N. B., Brohawn, K. H., Hughes, K. C., Macklin, M. L., Gold, A. L., Karpf, R. D., Orr, S. P., et al. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.09121812 · Cited by 170 · see citing works
Emotional enhancement of memory via amygdala-driven facilitation of rhinal interactions
Paz, R., Pelletier, J. G., Bauer, E. P., & Paré, D. (2006) · Nature Neuroscience · doi:10.1038/nn1771 · Cited by 167 · see citing works
Self-citationNeural Correlates of Variations in Event Processing during Learning in Basolateral Amygdala
Roesch, M. R., Calu, D. J., Esber, G. R., & Schoenbaum, G. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5781-09.2010 · Cited by 150 · see citing works
Attention for Learning Signals in Anterior Cingulate Cortex
Bryden, D. W., Johnson, E. E., Tobia, S. C., Kashtelyan, V., & Roesch, M. R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4715-11.2011 · Cited by 148 · see citing works
Hartley, C. A., Fischl, B., & Phelps, E. A. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq253 · Cited by 143 · see citing works
Dunsmoor, J. E., Bandettini, P. A., & Knight, D. C. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.4.635 · Cited by 137 · see citing works
Laurent, V., & Westbrook, R. F. (2008) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.1080108 · Cited by 133 · see citing works
Pannu Hayes, J., LaBar, K. S., Petty, C. M., McCarthy, G., & Morey, R. A. (2009) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2008.05.005 · Cited by 130 · see citing works
Muigg, P., Hetzenauer, A., Hauer, G., Hauschild, M., Gaburro, S., Frank, E., Landgraf, R., & Singewald, N. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06511.x · Cited by 119 · see citing works
A cingulo-amygdaloid projection in the rhesus monkey
Pandya, D. Ν., Hoesen, G. W. V., & Domesick, V. B. (1973) · Brain Research · doi:10.1016/0006-8993(73)90540-4 · Cited by 117 · see citing works
Laurent, V., Marchand, A., & Westbrook, R. F. (2008) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.928208 · Cited by 114 · see citing works
Narayanan, V., Heiming, R. S., Jansen, F., Lesting, J., Sachser, N., Pape, H.-C., & Seidenbecher, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022600 · Cited by 103 · see citing works
Sangha, S., Narayanan, R. T., Bergado-Acosta, J. R., Stork, O., Seidenbecher, T., & Pape, H. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2620-09.2009 · Cited by 99 · see citing works
Haselgrove, M., Aydin, A., & Pearce, J. M. (2004) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.30.3.240 · Cited by 85 · see citing works
Learning-Related Facilitation of Rhinal Interactions by Medial Prefrontal Inputs
Paz, R., Bauer, E. P., & Paré, D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1077-07.2007 · Cited by 72 · see citing works
Self-citationPartial reinforcement effects in classical aversive conditioning in rabbits and human beings.
Leonard, D. W. (1975) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0076419 · Cited by 58 · see citing works
Klavir, O., Genud-Gabai, R., & Paz, R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6481-11.2012 · Cited by 42 · see citing works
Self-citationLivneh, U., & Paz, R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0323-12.2012 · Cited by 34 · see citing works
Self-citationPartial reinforcement reduces the associative change produced by nonreinforcement.
Rescorla, R. A. (1999) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.25.4.403 · Cited by 24 · see citing works
Paz, R., Bauer, E. P., & Paré, D. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91259.2008 · Cited by 23 · see citing works
Self-citationPartial reinforcement reduces the associative change produced by nonreinforcement.
Rescorla, R. A. (1999) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.25.4.403 · Cited by 19 · see citing works
Livneh, U., & Paz, R. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.07.027 · Cited by 14 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Resolving the neural circuits of anxiety
Calhoon, G. G., & Tye, K. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4101 · Cited by 766 · see citing works
Emotion and the prefrontal cortex: an integrative review
Dixon, M. L., Thiruchselvam, R., Todd, R., & Christoff, K. (2017) · Psychological Bulletin · doi:10.1037/bul0000096 · Cited by 745 · see citing works
Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression
Courtin, J., Chaudun, F., Rozeske, R. R., Karalis, N., Gonzalez-Campo, C., Wurtz, H., Abdi, A., Baufreton, J., Bienvenu, T. C. M., & Herry, C. (2014) · Nature · doi:10.1038/nature12755 · Cited by 524 · see citing works
Fear Generalization and Anxiety: Behavioral and Neural Mechanisms
Dunsmoor, J. E., & Paz, R. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.04.010 · Cited by 499 · see citing works
Self-citationEncoding of fear learning and memory in distributed neuronal circuits
Herry, C., & Johansen, J. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3869 · Cited by 474 · see citing works
4-Hz oscillations synchronize prefrontal–amygdala circuits during fear behavior
Karalis, N., Déjean, C., Chaudun, F., Khoder, S., Rozeske, R. R., Wurtz, H., Bagur, S., Benchenane, K., Sirota, A., Courtin, J., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4251 · Cited by 379 · see citing works
Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment
Burgos-Robles, A., Kimchi, E. Y., Izadmehr, E. M., Porzenheim, M. J., Ramos-Guasp, W. A., Nieh, E. H., Felix-Ortiz, A. C., Namburi, P., Leppla, C. A., Presbrey, K. N., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4553 · Cited by 318 · see citing works
Impact of anxiety on prefrontal cortex encoding of cognitive flexibility
Park, J., & Moghaddam, B. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2016.06.013 · Cited by 218 · see citing works
Prefrontal neuronal assemblies temporally control fear behaviour
Déjean, C., Courtin, J., Karalis, N., Chaudun, F., Wurtz, H., Bienvenu, T., & Herry, C. (2016) · Nature · doi:10.1038/nature18630 · Cited by 216 · see citing works
Prefrontal cortical regulation of fear learning
Gilmartin, M. R., Balderston, N. L., & Helmstetter, F. J. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.05.004 · Cited by 197 · see citing works
Amygdala–prefrontal interactions in (mal)adaptive learning
Likhtik, E., & Paz, R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2014.12.007 · Cited by 193 · see citing works
Self-citationLong-Range Neural Synchrony in Behavior
Harris, A. Z., & Gordon, J. A. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034111 · Cited by 165 · see citing works
Gunnar, M. R., Hostinar, C. E., Sanchez, M. M., Tottenham, N., & Sullivan, R. M. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1070198 · Cited by 158 · see citing works
Marin, M., Zsido, R. G., Song, H., Lasko, N. B., Killgore, W. D. S., Rauch, S. L., Simon, N. M., & Milad, M. R. (2017) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2017.0329 · Cited by 151 · see citing works
Prefrontal-Periaqueductal Gray-Projecting Neurons Mediate Context Fear Discrimination
Rozeske, R. R., Jercog, D., Karalis, N., Chaudun, F., Khoder, S., Girard, D., Winke, N., & Herry, C. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.044 · Cited by 143 · see citing works
Afferents to anterior cingulate areas 24a and 24b and midcingulate areas 24a′ and 24b′ in the mouse
Fillinger, C., Yalçın, İ., Barrot, M., & Veinante, P. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1290-1 · Cited by 139 · see citing works
Functional Connectivity between Amygdala and Cingulate Cortex for Adaptive Aversive Learning
Klavir, O., Genud-Gabai, R., & Paz, R. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.035 · Cited by 120 · see citing works
Self-citationBehavioral and Neural Mechanisms of Overgeneralization in Anxiety
Laufer, O., Israeli, D., & Paz, R. (2016) · Current Biology · doi:10.1016/j.cub.2016.01.023 · Cited by 121 · see citing works
Self-citationLesting, J., Daldrup, T., Narayanan, V., Himpe, C., Seidenbecher, T., & Pape, H.-C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077707 · Cited by 105 · see citing works
Gee, D. G. (2016) · New Directions for Child and Adolescent Development · doi:10.1002/cad.20166 · Cited by 104 · see citing works
Efferents of anterior cingulate areas 24a and 24b and midcingulate areas 24aʹ and 24bʹ in the mouse
Fillinger, C., Yalçın, İ., Barrot, M., & Veinante, P. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1585-x · Cited by 97 · see citing works
Medial prefrontal cortex neuronal circuits in fear behavior
Courtin, J., Bienvenu, T., Einarsson, E. Ö., & Herry, C. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.001 · Cited by 97 · see citing works
Oscillations Synchronize Amygdala-to-Prefrontal Primate Circuits during Aversive Learning
Taub, A. H., Perets, R., Kahana, E., & Paz, R. (2017) · Neuron · doi:10.1016/j.neuron.2017.11.042 · Cited by 91 · see citing works
Self-citationTheta oscillations synchronize human medial prefrontal cortex and amygdala during fear learning
Chen, S., Tan, Z., Xia, W., Gomes, C. A., Zhang, X., Zhou, W., Liang, S., Axmacher, N., & Wang, L. (2021) · Science Advances · doi:10.1126/sciadv.abf4198 · Cited by 91 · see citing works
Brain activation during fear extinction predicts exposure success
Ball, T. M., Knapp, S. E., Paulus, M. P., & Stein, M. B. (2016) · Depression and Anxiety · doi:10.1002/da.22583 · Cited by 94 · see citing works
New learning and unlearning: strangers or accomplices in threat memory attenuation?
Clem, R. L., & Schiller, D. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.03.003 · Cited by 90 · see citing works
Fear generalization in the primate amygdala
Resnik, J., & Paz, R. (2014) · Nature Neuroscience · doi:10.1038/nn.3900 · Cited by 83 · see citing works
Self-citationVytal, K. E., Overstreet, C. M., Charney, D. R., Robinson, O. J., & Grillon, C. (2014) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.130145 · Cited by 82 · see citing works
Self-monitoring of social facial expressions in the primate amygdala and cingulate cortex
Livneh, U., Resnik, J., Shohat, Y., & Paz, R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207662109 · Cited by 78 · see citing works
Self-citationBrain activation induced by chronic psychosocial stress in mice
Laine, M. A., Sokolowska, E., Dudek, M., Callan, S., Hyytiä, P., & Hovatta, I. (2017) · Scientific Reports · doi:10.1038/s41598-017-15422-5 · Cited by 76 · see citing works
A Tradeoff in the Neural Code across Regions and Species
Pryluk, R., Kfir, Y., Gelbard-Sagiv, H., Fried, I., & Paz, R. (2019) · Cell · doi:10.1016/j.cell.2018.12.032 · Cited by 72 · see citing works
Self-citationBasolateral Amygdala Neurons Maintain Aversive Emotional Salience
Sengupta, A., Yau, J. O.-Y., Jean-Richard-dit-Bressel, P., Liu, Y., Millan, E. Z., Power, J., & McNally, G. P. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2460-17.2017 · Cited by 71 · see citing works
Physiological basis for emotional modulation of memory circuits by the amygdala
Paz, R., & Paré, D. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.008 · Cited by 69 · see citing works
Self-citationWen, Z., Seo, J., Pace-Schott, E. F., & Milad, M. R. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01462-5 · Cited by 62 · see citing works
Conserved features of anterior cingulate networks support observational learning across species
Burgos-Robles, A., Gothard, K. M., Monfils, M., Morozov, A., & Vicentic, A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.009 · Cited by 60 · see citing works
Çalışkan, G., & Stork, O. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.02.022 · Cited by 55 · see citing works
Safety Signals in the Primate Amygdala
Genud-Gabai, R., Klavir, O., & Paz, R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1539-13.2013 · Cited by 56 · see citing works
Self-citationMorriss, J., & van Reekum, C. M. (2019) · Behaviour Research and Therapy · doi:10.1016/j.brat.2019.03.004 · Cited by 46 · see citing works
Morriss, J., Saldarini, F., Chapman, C., Pollard, M. I., & van Reekum, C. M. (2019) · Journal of Experimental Psychopathology · doi:10.1177/2043808719834451 · Cited by 45 · see citing works
Carlisi, C. O., & Robinson, O. J. (2018) · Brain and Neuroscience Advances · doi:10.1177/2398212818774223 · Cited by 42 · see citing works
Lateral, not medial, prefrontal cortex contributes to punishment and aversive instrumental learningPreprint
Jean-Richard-dit-Bressel, P., & McNally, G. P. (2016) · Learning & Memory · doi:10.1101/lm.042820.116 · Cited by 41 · see citing works
The role of threat level and intolerance of uncertainty in extinction
Morriss, J., Saldarini, F., & van Reekum, C. M. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2019.05.013 · Cited by 39 · see citing works
The cerebellum regulates fear extinction through thalamo-prefrontal cortex interactions in male mice
Frontera, J. L., Sala, R. W., Georgescu, I. A., Baba Aissa, H., d’Almeida, M. N., Popa, D., & Léna, C. (2023) · Nature Communications · doi:10.1038/s41467-023-36943-w · Cited by 38 · see citing works
Physiological Signature of Memory Age in the Prefrontal-Hippocampal Circuit
Makino, Y., Polygalov, D., Bolaños, F., Benucci, A., & McHugh, T. J. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.11.075 · Cited by 36 · see citing works
Aversive learning strengthens episodic memory in both adolescents and adultsPreprint
Cohen, A. O., Matese, N. G., Filimontseva, A., Shen, X., Shi, T. C., Livne, E., & Hartley, C. A. (2019) · Learning & Memory · doi:10.1101/lm.048413.118 · Cited by 36 · see citing works
Kuhn, M., Weidenauer, A., & Pezawas, L. (2014) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-139005 · Cited by 35 · see citing works
Brain Mechanisms Controlling Pavlovian Fear Conditioning
Yau, J., & McNally, G. (2018) · Journal of Experimental Psychology: Animal Learning and Cognition · doi:10.1037/xan0000181 · Cited by 23 · see citing works
Gao, W., Biswal, B. B., Chen, S., Wu, X., & Yuan, J. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.117918 · Cited by 30 · see citing works
Expanding the canon: An inclusive neurobiology of thalamic and subthalamic fear circuits
Venkataraman, A., & Dias, B. G. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109380 · Cited by 26 · see citing works
Approaches to inferring multi-regional interactions from simultaneous population recordings
Kang, B., & Druckmann, S. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.10.004 · Cited by 27 · see citing works
The effect of social anxiety on the acquisition and extinction of low-cost avoidance
Wake, S., van Reekum, C. M., & Dodd, H. F. (2021) · Behaviour Research and Therapy · doi:10.1016/j.brat.2021.103967 · Cited by 19 · see citing works
Neural Oscillatory Correlates for Conditioning and Extinction of Fear
Trenado, C., Pedroarena‐Leal, N., Cif, L., Nitsche, M. A., & Ruge, D. (2018) · Biomedicines · doi:10.3390/biomedicines6020049 · Cited by 23 · see citing works
Manning, E. E., Bradfield, L. A., & Iordanova, M. (2020) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.030 · Cited by 16 · see citing works
Déjean, C., Sitko, M., Girardeau, P., Bennabi, A., Caillé, S., Cador, M., Boraud, T., & Moine, C. L. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.272 · Cited by 20 · see citing works
Sonic hedgehog signaling regulates amygdalar neurogenesis and extinction of fear memory
Hung, H.-C., Hsiao, Y., & Gean, P. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.07.005 · Cited by 19 · see citing works
Uncertainty-Dependent Extinction of Fear Memory in an Amygdala-mPFC Neural Circuit Model
Li, Y., Nakae, K., Ishii, S., & Naoki, H. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005099 · Cited by 18 · see citing works
Reliability of fronto–amygdala coupling during emotional face processing
Nord, C., Gray, A., Robinson, O., & Roiser, J. (2019) · Brain Sciences · doi:10.3390/brainsci9040089 · Cited by 17 · see citing works
Affective memory rehearsal with temporal sequences in amygdala neurons
Reitich-Stolero, T., & Paz, R. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0542-9 · Cited by 17 · see citing works
Self-citationKirry, A. J., Twining, R. C., & Gilmartin, M. R. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107249 · Cited by 16 · see citing works
Bierwirth, P., Antov, M. I., & Stockhorst, U. (2023) · Psychophysiology · doi:10.1111/psyp.14283 · Cited by 16 · see citing works
Long time-scales in primate amygdala neurons support aversive learning
Taub, A. H., Reitich-Stolero, T., Livneh, U., Shohat, Y., & Paz, R. (2018) · Nature Communications · doi:10.1038/s41467-018-07020-4 · Cited by 14 · see citing works
Self-citationSocial processing by the primate medial frontal cortex
Putnam, P. T., & Chang, S. W. C. (2021) · International review of neurobiology · doi:10.1016/bs.irn.2020.12.003 · Cited by 18 · see citing works
The influence of self-awareness on emotional memory formation: an fMRI study
Pais-Vieira, C., Wing, E. A., & Cabeza, R. E. L. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv141 · Cited by 15 · see citing works
Yan, R., Wang, T., Ma, X., Zhang, X., Zheng, R., & Zhou, Q. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109503 · Cited by 12 · see citing works
Tobore, T. O. (2018) · Psychological Reports · doi:10.1177/0033294118792670 · Cited by 11 · see citing works
Neural Circuits for Fear Relapse
Goode, T. D., Jin, J., & Maren, S. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813693-5.00010-1 · Cited by 9 · see citing works
Neuronal theta oscillation of hippocampal ensemble and memory function
Sun, L., & Bao, L. (2025) · Behavioural Brain Research · doi:10.1016/j.bbr.2025.115429 · Cited by 8 · see citing works
Herry, C., & Jercog, D. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102600 · Cited by 7 · see citing works
Lewis, V., Laberge, F., & Heyland, A. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107502 · Cited by 6 · see citing works
Ghane, M., Trambaiolli, L. R., Bertocci, M. A., Martínez-Rivera, F. J., Chase, H. W., Brady, T., Skeba, A., Graur, S., Bonar, L. K., Iyengar, S., et al. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.12.027 · Cited by 6 · see citing works
Li, S. S. Y., & McNally, G. P. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12892 · Cited by 6 · see citing works
Samuel, N., Kahana, E., Taub, A. H., Reitich-Stolero, T., Paz, R., & Raz, A. (2021) · Anesthesiology · doi:10.1097/aln.0000000000003732 · Cited by 6 · see citing works
Self-citationRate and noise in human amygdala drive increased exploration in aversive learning
Reitich-Stolero, T., Aberg, K. C., Halperin, D., Ariel, C., Morris, G., Goldstein, L., Fahoum, F., Strauss, I., & Paz, R. (2025) · Nature · doi:10.1038/s41586-025-09466-1 · Cited by 5 · see citing works
Self-citationCranston, C. C. (2014) · The New School psychology bulletin · Cited by 2 · see citing works
It All Depends on the Context, but Also on the Amygdala
Cohen, Y., & Paz, R. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.012 · Cited by 2 · see citing works
Self-citationMaladaptive learning and the amygdala—prefrontal circuit
Likhtik, E., & Paz, R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813983-7.00021-5 · Cited by 2 · see citing works
Self-citationShohat, Y., Paz, R., Pryluk, R., & Taub, A. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/803528 · Cited by 1 · see citing works
Self-citationEtiological Factors: Basic Neuroscience
Cohodes, E. M., & Gee, D. G. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813004-9.00004-9 · Cited by 1 · see citing works
Stable coding of aversive associations in medial prefrontal populations
Herry, C., & Jercog, D. (2023) · Comptes Rendus Biologies · doi:10.5802/crbiol.126
Polygenic prediction of fear learning is mediated by brain connectivityPreprint
Penate, J. S., Gomes, C. A., Spisák, T., Genç, E., Merz, C. J., Wolf, O. T., Quick, H. H., Elsenbruch, S., Engler, H., Fraenz, C., et al. (2025) · medRxiv · doi:10.1101/2025.03.12.25323754
Kim, J., Halverson, H. E., & Freeman, J. H. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0142-25.2025
Neural Mechanisms in Primates Underlying Short- and Long-Term SSRI EffectsPreprint
Iskhakova, L., Perets, R., Yariv, S., & Paz, R. (2025) · Research Square · doi:10.21203/rs.3.rs-7223004/v1
Self-citationSridhar, S., Biagi, N., & Wake, S. (2026) · Behaviour Research and Therapy · doi:10.1016/j.brat.2026.105088
- Authors
- Livneh, U., & Paz, R.
- Affiliations
- Weizmann Institute of Science (IL)
- Corresponding author
- Paz, Rony
- ORCID
- Paz, Rony
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2012-07
- Volume
- 75
- Issue
- 1
- Pages
- 133-142
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W1972504466
- Cited by
- 87
- References
- 61
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 7 · 2020: 3 · 2019: 12 · 2018: 8 · 2017: 9 · 2016: 12 · 2015: 9 · 2014: 6 · 2013: 6 · 2012: 1
- FWCI
- 3.60
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute for Psychobiology in Israel, Hebrew University of Jerusalem
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- memory extinction, aversive memory, memory persistence, amygdala, dorsal anterior cingulate cortex, neuronal synchronization, partial reinforcement extinction effect, continuous reinforcement, distributed representations, neural correlates of memory, monkeys
- MeSH terms
- Amygdala, Animals, Avoidance Learning, Conditioning, Psychological, Extinction, Psychological, Macaca fascicularis, Male, Memory, Neural Pathways, Reinforcement Schedule, Prefrontal Cortex
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
