Auditory-Evoked Spike Firing in the Lateral Amygdala and Pavlovian Fear Conditioning
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Amygdala neuroplasticity has emerged as a candidate substrate for Pavlovian fear memory. By this view, conditional stimulus (CS)-evoked activity represents a mnemonic code that initiates the expression of fear behaviors. However, a fear state may nonassociatively enhance sensory processing, biasing CS-evoked activity in amygdala neurons. Here we describe experiments that dissociate auditory CS-evoked spike firing in the lateral amygdala (LA) and both conditional fear behavior and LA excitability in rats. We found that the expression of conditional freezing and increased LA excitability was neither necessary nor sufficient for the expression of conditional increases in CS-evoked spike firing. Rather, conditioning-related changes in CS-evoked spike firing were solely determined by the associative history of the CS. Thus, our data support a model in which associative activity in the LA encodes fear memory and contributes to the expression of learned fear behaviors.
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Several lines of indirect evidence support the idea that this plasticity occurs as a result of a Hebbian mechanism through which depolarization of LA pyramidal neurons by the shock US coincident with weaker activation of the same cells by auditory CS inputs results in fear learning.
“Several lines of indirect evidence support the idea that this plasticity occurs as a result of a Hebbian mechanism through which depolarization of LA pyramidal neurons by the shock US coincident with weaker activation of the same cells by auditory CS inputs results in fear learning (8–18).”
From Optical activation of lateral amygdala pyramidal cells instructs associative fear learning (2010) · cites this paper as [11]
Cites
The amygdala: vigilance and emotion
Davis, M., & Whalen, P. J. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000812 · Cited by 2,882 · see citing works
The role of the amygdala in fear and anxiety
Davis, M. (1992) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.15.030192.002033 · Cited by 2,357 · see citing works
Brain Maps: Structure of the Rat Brain
Swanson, L. W. (1992) · Medical Entomology and Zoology · Cited by 1,851 · see citing works
Neurobiology of Pavlovian Fear Conditioning
Maren, S. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.897 · Cited by 1,805 · see citing works
Self-citationLeDoux, J., Iwata, J., Cicchetti, P., & Reis, D. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-07-02517.1988 · Cited by 1,580 · see citing works
Fear conditioning induces associative long-term potentiation in the amygdala
Rogan, M. T., Stäubli, U. V., & LeDoux, J. E. (1997) · Nature · doi:10.1038/37601 · Cited by 1,310 · see citing works
The neuroanatomical and neurochemical basis of conditioned fear
Fendt, M., & Fanselow, M. S. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00016-0 · Cited by 1,092 · see citing works
Why We Think Plasticity Underlying Pavlovian Fear Conditioning Occurs in the Basolateral Amygdala
Fanselow, M. S., & LeDoux, J. E. (1999) · Neuron · doi:10.1016/s0896-6273(00)80775-8 · Cited by 914 · see citing works
Quirk, G. J., Repa, J. C., & LeDoux, J. E. (1995) · Neuron · doi:10.1016/0896-6273(95)90092-6 · Cited by 808 · see citing works
Amygdala circuitry in attentional and representational processes.
Holland, P., & Gallagher, M. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(98)01271-6 · Cited by 613 · see citing works
Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning
Blair, H. T., Schafe, G. E., Bauer, E. P., Rodrigues, S. M., & LeDoux, J. E. (2001) · Learning & Memory · doi:10.1101/lm.30901 · Cited by 610 · see citing works
Quirk, G. J., Armony, J. L., & LeDoux, J. E. (1997) · Neuron · doi:10.1016/s0896-6273(00)80375-x · Cited by 563 · see citing works
Attentional control of the processing of neutral and emotional stimuli
Pessoa, L., Kästner, S., & Ungerleider, L. G. (2002) · Cognitive Brain Research · doi:10.1016/s0926-6410(02)00214-8 · Cited by 525 · see citing works
Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo
Maren, S., & Fanselow (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07548.1995 · Cited by 499 · see citing works
Self-citationLong-term potentiation in the amygdala: a mechanism for emotional learning and memory
Maren, S. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01465-4 · Cited by 456 · see citing works
Self-citationTwo different lateral amygdala cell populations contribute to the initiation and storage of memory
Repa, J. C., Muller, J., Apergis, J., Desrochers, T. M., Zhou, Y., & LeDoux, J. E. (2001) · Nature Neuroscience · doi:10.1038/89512 · Cited by 440 · see citing works
Intrinsic connections of the rat amygdaloid complex: Projections originating in the basal nucleus
Savander, V., Go, C. ‐., LeDoux, J. E., & Pitkänen, A. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903610211 · Cited by 416 · see citing works
The Amygdala and Fear Conditioning: Has the Nut Been Cracked?
Maren, S., & Fanselow, M. S. (1996) · Neuron · doi:10.1016/s0896-6273(00)80041-0 · Cited by 407 · see citing works
Self-citationClassical fear conditioning in functional neuroimaging
Büchel, C. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00078-7 · Cited by 350 · see citing works
Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning
Rosenkranz, J. A., & Grace, A. A. (2002) · Nature · doi:10.1038/417282a · Cited by 348 · see citing works
Electrophysiological and morphological properties of rat basolateral amygdaloid neurons in vitro
Washburn, M., & Moises, H. C. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-10-04066.1992 · Cited by 270 · see citing works
Amygdaloid contributions to conditioned arousal and sensory information processing.
Kapp, B. S., Whalen, P. J., Supple, W. F., & Pascoe, J. P. (1992) · Cited by 265 · see citing works
Neuronal transmission through hippocampal pathways dependent on behavior
Winson, J., & Abzug, C. (1978) · Journal of Neurophysiology · doi:10.1152/jn.1978.41.3.716 · Cited by 262 · see citing works
Paré, D., & Collins, D. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02701.2000 · Cited by 262 · see citing works
Is the Amygdala a Locus of “Conditioned Fear”? Some Questions and Caveats
Cahill, L. F., Weinberger, N. M., Roozendaal, B., & McGaugh, J. L. (1999) · Neuron · doi:10.1016/s0896-6273(00)80774-6 · Cited by 249 · see citing works
Petrovich, G. D., & Swanson, L. W. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01361-3 · Cited by 234 · see citing works
Paré, D., & Gaudreau, H. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03334.1996 · Cited by 230 · see citing works
Sananes, C. B., & Davis, M. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.72 · Cited by 216 · see citing works
Kapp, B. S., Gallagher, M., Underwood, M. D., McNall, C. L., & Whitehorn, D. (1982) · Brain Research · doi:10.1016/0006-8993(82)90866-6 · Cited by 208 · see citing works
Hobin, J. A., Goosens, K. A., & Maren, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08410.2003 · Cited by 187 · see citing works
Self-citationMaren, S., Yap, S. A., & Goosens, K. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-06-j0001.2001 · Cited by 186 · see citing works
Self-citationHitchcock, J. M., Sananes, C. B., & Davis, M. (1989) · Behavioral Neuroscience · doi:10.1037//0735-7044.103.3.509 · Cited by 180 · see citing works
Collins, D. R., & Paré, D. (2000) · Learning & Memory · doi:10.1101/lm.7.2.97 · Cited by 171 · see citing works
Amygdala, hippocampus and discriminative fear conditioning to context
Antoniadis, E. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00121-7 · Cited by 170 · see citing works
Sananes, C. B., & Davis, M. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.1.72 · Cited by 164 · see citing works
Discriminative fear conditioning to context expressed by multiple measures of fear in the rat
Antoniadis, E. A., & McDonald, R. J. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00056-4 · Cited by 151 · see citing works
Applegate, C. D., Frysinger, R. C., Kapp, B. S., & Gallagher, M. (1982) · Brain Research · doi:10.1016/0006-8993(82)90123-8 · Cited by 147 · see citing works
Hitchcock, J. M., Sananes, C. B., & Davis, M. T. (1989) · Behavioral Neuroscience · doi:10.1037/0735-7044.103.3.509 · Cited by 145 · see citing works
Maren, S. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00281.x · Cited by 139 · see citing works
Self-citationFear conditioning and LTP in the lateral amygdala are sensitive to the same stimulus contingencies
Bauer, E. P., LeDoux, J. E., & Nader, K. (2001) · Nature Neuroscience · doi:10.1038/89465 · Cited by 112 · see citing works
Goosens, K. A., & Maren, S. (2002) · Hippocampus · doi:10.1002/hipo.10099 · Cited by 104 · see citing works
Self-citationMaren, S., Poremba, A., & Michael, G. (1991) · Brain Research · doi:10.1016/0006-8993(91)90473-9 · Cited by 96 · see citing works
Self-citationLesions of the Amygdala Central Nucleus Alter Performance on a Selective Attention Task
Holland, P. C., Han, J., & Gallagher, M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06701.2000 · Cited by 90 · see citing works
Amygdalar Efferents Initiate Auditory Thalamic Discriminative Training-Induced Neuronal Activity
Poremba, A., & Gabriel, M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00270.2001 · Cited by 82 · see citing works
Neural systems for the expression of hypoalgesia during nonassociative fear.
Bellgowan, P. S. F., & Helmstetter, F. J. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.4.727 · Cited by 76 · see citing works
McEchron, M. D., McCabe, P. M., Green, E. J., Llabre, M. M., & Schneiderman, N. (1995) · Brain Research · doi:10.1016/0006-8993(95)00331-j · Cited by 70 · see citing works
Neural systems for the expression of hypoalgesia during nonassociative fear.
Bellgowan, P. S. F., & Helmstetter, F. J. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.4.727 · Cited by 69 · see citing works
Tang, J., Wotjak, C. T., Wagner, S., Williams, G., Schachner, M., & Dityatev, A. E. (2001) · Brain Research · doi:10.1016/s0006-8993(01)03020-7 · Cited by 39 · see citing works
Mechanisms of Pavlovian fear conditioning: has the engram been located?
Paré, D. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02243-9 · Cited by 30 · see citing works
Bilak, S. R., & Morest, D. K. (1998) · Synapse · doi:10.1002/(sici)1098-2396(199804)28:4 · Cited by 28 · see citing works
Short-latency discriminative unit response: Engram or bias?
Gabriel, M. (1976) · Physiological Psychology · doi:10.3758/bf03332870 · Cited by 25 · see citing works
Does the basolateral amygdala store memories for emotional events?
Vazdarjanova, A. I. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01599-x · Cited by 25 · see citing works
The amygdala and associative learning
Gallagher, M. (2000) · doi:10.1093/oso/9780198505013.003.0008 · Cited by 24 · see citing works
Ashe, J. H., Cassady, J. M., & Weinberger, N. M. (1976) · Behavioral Biology · doi:10.1016/s0091-6773(76)91108-1 · Cited by 16 · see citing works
Response: Mechanisms of Pavlovian fear conditioning
Rosenkranz, J. A., & Grace, A. A. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02239-7 · Cited by 4 · see citing works
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Maren, S., & Quirk, G. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1535 · Cited by 1,428 · see citing works
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Duvarci, S., & Pare, D. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.042 · Cited by 751 · see citing works
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Self-citationAmbroggi, F., Ishikawa, A., Fields, H. L., & Nicola, S. M. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.004 · Cited by 488 · 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
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Self-citationEmotional Perseveration: An Update on Prefrontal-Amygdala Interactions in Fear ExtinctionPreprint
Sotres-Bayón, F., Bush, D. E. A., & LeDoux, J. E. (2004) · Learning & Memory · doi:10.1101/lm.79504 · Cited by 407 · see citing works
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Corcoran, K., Desmond, T., Frey, K., & Maren, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2246-05.2005 · Cited by 390 · see citing works
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Grewe, B. F., Gründemann, J., Kitch, L. J., Lecoq, J. A., Parker, J. G., Marshall, J. D., Larkin, M. C., Jercog, P. E., Grenier, F., Li, J. Z., et al. (2017) · Nature · doi:10.1038/nature21682 · Cited by 351 · see citing works
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Sigurdsson, T., Doyère, V., Cain, C. K., & LeDoux, J. E. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.022 · Cited by 325 · see citing works
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Maren, S. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.023 · Cited by 259 · see citing works
“‘‘Fear’’ neurons responded to nonextinguished CSs or extinguished CSs presented outside the extinction context, whereas extinction neurons only responded to extinguished CSs presented in their Neuron 70, June 9, 2011 ª2011 Elsevier Inc. 833 LA IT C CEl CEm IL PL HIP low fear BA Extinction context LA IT C CEl CEm IL PL…”
BackgroundInfluentialSelf-citationDistinct Neural Signatures for Safety and Danger in the Amygdala and Striatum of the Mouse
Rogan, M. T., Leon, K. S., Perez, D. L., & Kandel, E. R. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.017 · Cited by 226 · see citing works
Amygdala ensembles encode behavioral states
Gründemann, J., Bitterman, Y., Lu, T., Krabbe, S., Grewe, B. F., Schnitzer, M. J., & Lüthi, A. (2019) · Science · doi:10.1126/science.aav8736 · Cited by 223 · see citing works
Rosen, J. B. (2004) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582304265945 · Cited by 219 · see citing works
Cannabinoid CB1 Receptor Mediates Fear Extinction via Habituation-Like Processes
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Serotonin, Amygdala and Fear: Assembling the Puzzle
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Encoding of Discriminative Fear Memory by Input-Specific LTP in the Amygdala
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Ramirez, F., Moscarello, J. M., LeDoux, J. E., & Sears, R. M. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1331-14.2015 · Cited by 198 · see citing works
Shabel, S. J., & Janak, P. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905580106 · Cited by 190 · see citing works
Ji, J.-Z., & Maren, S. (2008) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.794808 · Cited by 195 · see citing works
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Maren, S. (2005) · The Neuroscientist · doi:10.1177/1073858404269232 · Cited by 160 · see citing works
Self-citationSah, P., Westbrook, R. F., & Lüthi, A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1417.020 · Cited by 138 · see citing works
Memory recall and modifications by activating neurons with elevated CREB
Kim, J., Kwon, J.-T., Kim, H.-S., Josselyn, S. A., & Han, J. (2013) · Nature Neuroscience · doi:10.1038/nn.3592 · Cited by 136 · see citing works
Hippocampal regulation of context-dependent neuronal activity in the lateral amygdala.Preprint
Maren, S., & Hobin, J. A. (2007) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.477007 · Cited by 128 · see citing works
Self-citationChemosignals of Fear Enhance Cognitive Performance in Humans
Chen, D. (2006) · Chemical Senses · doi:10.1093/chemse/bjj046 · Cited by 121 · see citing works
Goosens, K. A., & Maren, S. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03513.x · Cited by 108 · see citing works
Self-citationPositive and negative ultrasonic social signals elicit opposing firing patterns in rat amygdala
Parsana, A. J., Li, N., & Brown, T. H. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.040 · Cited by 108 · see citing works
Chang, C., Berke, J. D., & Maren, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011971 · Cited by 105 · see citing works
Self-citationHeterosynaptic Long-Term Potentiation of Inhibitory Interneurons in the Lateral Amygdala
Bauer, E. P., & LeDoux, J. E. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3567-04.2004 · Cited by 105 · see citing works
Noradrenergic blockade stabilizes prefrontal activity and enables fear extinction under stress
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Self-citationNature and causes of the immediate extinction deficit: A brief review
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Self-citationRetrieving fear memories, as time goes by…
Monte, F. H. D., Quirk, G. J., Li, B., & Penzo, M. A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.78 · Cited by 95 · see citing works
Fear conditioning and the basolateral amygdala
Sun, Y., Gooch, H., & Sah, P. (2020) · F1000Research · doi:10.12688/f1000research.21201.1 · Cited by 104 · see citing works
Sevelinges, Y., Gervais, R., Messaoudi, B., Granjon, L., & Mouly, A. (2004) · Learning & Memory · doi:10.1101/lm.83604 · Cited by 91 · see citing works
Haaker, J., Maren, S., Andreatta, M., Merz, C. J., Richter, J., Richter, S. H., Drexler, S. M., Lange, M. D., Jüngling, K., Nees, F., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.020 · Cited by 89 · see citing works
Self-citationAmygdala, Long-term Potentiation, and Fear Conditioning
Dityatev, A. E., & Bolshakov, V. Y. (2005) · The Neuroscientist · doi:10.1177/1073858404270857 · Cited by 85 · see citing works
Review of salicylate-induced hearing loss, neurotoxicity, tinnitus and neuropathophysiology.
Sheppard, A., Hayes, S. H., Chen, G.-D., Ralli, M., & Salvi, R. (2014) · Europe PMC (PubMed Central) · Cited by 84 · see citing works
Dynamical prefrontal population coding during defensive behaviours
Jercog, D., Winke, N., Sung, K., Martín‐Fernández, M., Francioni, C., Rajot, D., Courtin, J., Chaudun, F., Jercog, P. E., Valério, S., et al. (2021) · Nature · doi:10.1038/s41586-021-03726-6 · Cited by 81 · see citing works
Mechanisms of fear learning and extinction: synaptic plasticity–fear memory connection
Luchkina, N. V., & Bolshakov, V. Y. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5104-4 · Cited by 77 · see citing works
Spatiotemporal asymmetry of associative synaptic plasticity in fear conditioning pathways.
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Paré, D., & Quirk, G. (2017) · npj Science of Learning · doi:10.1038/s41539-017-0007-4 · Cited by 71 · see citing works
Ensemble coding in amygdala circuits for associative learning
Gründemann, J., & Lüthi, A. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.10.005 · Cited by 66 · see citing works
van Rossum, E. F. C., Roks, P. H. M., de Jong, F. H., Brinkmann, A. O., Pols, H. A. P., Koper, J. W., & Lamberts, S. W. J. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02132.x · Cited by 60 · see citing works
Almada, R. C., Borelli, K. G., Albrechet‐Souza, L., & Brandão, M. L. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.05.017 · Cited by 59 · see citing works
Flexible Neural Representations of Value in the Primate Brain
Salzman, C. D., Paton, J. J., Belova, M. A., & Morrison, S. E. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1401.034 · Cited by 57 · see citing works
Dissociated Fear and Spatial Learning in Mice with Deficiency of Ataxin-2
Huynh, D. P., Maalouf, M., Silva, A. J., Schweizer, F. E., & Pulst, S. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006235 · Cited by 57 · see citing works
Kim, E. J., Kong, M.-S., Park, S. G., Mizumori, S., Cho, J., & Kim, J. J. (2018) · Science Advances · doi:10.1126/sciadv.aar7328 · Cited by 37 · see citing works
Dopaminergic modulation of spontaneous inhibitory network activity in the lateral amygdala
Lorétan, K., Bissière, S., & Lüthi, A. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.015 · Cited by 56 · see citing works
Pochwat, B., Sowa-Kućma, M., Kotarska, K., Misztak, P., Nowak, G., & Szewczyk, B. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3671-6 · Cited by 55 · see citing works
Perkowski, J. J., & Murphy, G. G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2634-10.2011 · Cited by 54 · see citing works
Long-Term Neural Correlates of Reversible Fear Learning in the Lateral Amygdala
An, B., Hong, I., & Choi, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3017-12.2012 · Cited by 54 · see citing works
Kim, D., Paré, D., & Nair, S. S. (2013) · Learning & Memory · doi:10.1101/lm.030262.113 · Cited by 52 · see citing works
Convergent Coding of Recent and Remote Fear Memory in the Basolateral Amygdala
Liu, J., Totty, M. S., Melissari, L., Bayer, H., & Maren, S. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.12.018 · Cited by 49 · see citing works
Self-citationHolschneider, D. P., Yang, J., Sadler, T. R., Nguyen, P. T., Givrad, T. K., & Maarek, J. M. I. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.08.038 · Cited by 47 · see citing works
Moses, S. N., Houck, J. M., Martin, T., Hanlon, F. M., Ryan, J. D., Thoma, R. J., Weisend, M. P., Jackson, E. M., Pekkonen, E., & Tesche, C. D. (2006) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.08.016 · Cited by 46 · see citing works
Asymmetrical stimulus generalization following differential fear conditioning
Bang, S. J., Allen, T. A., Jones, L. K., Boguszewski, P. M., & Brown, T. H. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.02.009 · Cited by 45 · see citing works
Current emotion research in behavioral neuroscience: the role(s) of the amygdala
Armony, J. L. (2013) · Emotion Review · doi:10.1177/1754073912457208 · Cited by 44 · see citing works
The dynamic nature of fear engrams in the basolateral amygdala
Davis, P. W., & Reijmers, L. G. J. E. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.12.004 · Cited by 41 · see citing works
Rorick‐Kehn, L. M., & Steinmetz, J. E. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.5.1254 · Cited by 41 · see citing works
Furtak, S. C., Allen, T. A., & Brown, T. H. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1653-07.2007 · Cited by 39 · see citing works
The amygdala: A potential player in timing CS–US intervals
Díaz-Mataix, L., Tallot, L., & Doyère, V. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.08.007 · Cited by 38 · see citing works
Role of the basolateral amygdala and NMDA receptors in higher-order conditioned fear
Parkes, S. L., & Westbrook, R. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.025 · Cited by 28 · see citing works
Kim, D., Samarth, P. S., Feng, F., Paré, D., & Nair, S. S. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1037-4 · Cited by 37 · see citing works
Barkus, C., Line, S. J., Huber, A., Capitão, L. P., Lima, J., Jennings, K. A., Lowry, J., Sharp, T., Bannerman, D. M., & McHugh, S. B. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.09.003 · Cited by 35 · see citing works
Input from the medial geniculate nucleus modulates amygdala encoding of fear memory discriminationPreprint
Ferrara, N. C., Cullen, P. K., Pullins, S. E., Rotondo, E. K., & Helmstetter, F. J. (2017) · Learning & Memory · doi:10.1101/lm.044131.116 · Cited by 37 · see citing works
Evaluation of ambiguous associations in the amygdala by learning the structure of the environment
Madarász, T. J., Díaz-Mataix, L., Akhand, O., Ycu, E. A., LeDoux, J. E., & Johansen, J. P. (2016) · Nature Neuroscience · doi:10.1038/nn.4308 · Cited by 30 · see citing works
Serotonergic neuromodulation of synaptic plasticity
Higa, G. S. V., Viana, F. J. C., Francis-Oliveira, J., Cruvinel, E., Franchin, T. S., Marcourakis, T., Ulrich, H., & De Pasquale, R. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110036 · Cited by 29 · see citing works
Trent, S., Abdullah, M. H., Parwana, K., Valdivieso, M. A., Hassan, Z., & Müller, C. P. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111310 · Cited by 26 · see citing works
Deciphering Memory Function with Optogenetics
Beyeler, A., Eckhardt, C. A., & Tye, K. M. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-420170-5.00012-x · Cited by 24 · see citing works
Kiyokawa, Y., Mikami, K., Mikamura, Y., Ishii, A., Takeuchi, Y., & Mori, Y. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.055 · Cited by 22 · see citing works
Dopaminergic circuits underlying associative aversive learning
Zafiri, D., & Duvarci, S. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1041929 · Cited by 23 · see citing works
Memory coding in plastic neuronal subpopulations within the amygdala
Nomura, H., Nonaka, A., HitoraーImamura, N., Hashikawa, K., & Matsuki, N. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.022 · Cited by 22 · see citing works
Kwon, J.-T., & Choi, J.-S. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5928-08.2009 · Cited by 20 · see citing works
Neuronal coding mechanisms mediating fear behavior
Rozeske, R. R., & Herry, C. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.04.017 · Cited by 21 · see citing works
McHugh, S. B., Marques–Smith, A., Li, J., Rawlins, J. N. P., Lowry, J., Conway, M. W., Gilmour, G., Tricklebank, M. D., & Bannerman, D. M. (2012) · European Journal of Neuroscience · doi:10.1111/ejn.12057 · Cited by 20 · see citing works
The Contribution of the Amygdala to Aversive and Appetitive Pavlovian Processes
Moscarello, J. M., & LeDoux, J. E. (2013) · Emotion Review · doi:10.1177/1754073913477508 · Cited by 20 · see citing works
Lee, S., Amir, A., Headley, D. B., Haufler, D., & Paré, D. (2016) · Nature Communications · doi:10.1038/ncomms12275 · Cited by 20 · see citing works
Learning rules for aversive associative memory formation
Ozawa, T., & Johansen, J. P. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.010 · Cited by 22 · see citing works
Inhibitory avoidance learning altered ensemble activity of amygdaloid neurons in rats
Chang, C., Liang, K., & Yen, C. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03821.x · Cited by 18 · see citing works
Du, Y., Wang, Q., Zhang, Y., Wu, X. H., & Li, L. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.022 · Cited by 16 · see citing works
Zafiri, D., Salinas-Hernández, X. I., Biasi, E. S. D., Rebelo, L., & Duvarci, S. (2025) · Nature Communications · doi:10.1038/s41467-025-58382-5 · Cited by 14 · see citing works
Almada, R. C., Albrechet‐Souza, L., & Brandão, M. L. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881113482840 · Cited by 14 · see citing works
Moratti, S., Giménez‐Fernández, T., Méndez‐Bértolo, C., & de Vicente-Perez, F. (2017) · Psychophysiology · doi:10.1111/psyp.12841 · Cited by 13 · see citing works
The Impact of Stressor Exposure and Glucocorticoids on Anxiety and Fear
Hassell, J. E., Nguyen, K., Gates, C. A., & Lowry, C. A. (2018) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_63 · Cited by 13 · see citing works
A model of amygdala function following plastic changes at specific synapses during extinction
Bennett, M. R., Farnell, L., Gibson, W. G., & Lagopoulos, J. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2019.100159 · Cited by 12 · see citing works
Integrating Aversive Memories in the Basolateral Amygdala
Liu, J., Totty, M. S., Bayer, H., & Maren, S. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.03.019 · Cited by 10 · see citing works
Self-citationHao, L., Yang, Z., Gong, P., & Lei, J. (2018) · Cognitive Neurodynamics · doi:10.1007/s11571-018-9479-z · Cited by 9 · see citing works
Inhibitory Fear Memory Engram in the Mouse Central Lateral Amygdala
Hou, W., Jariwala, M., Wang, K., Seewald, A., Lin, Y. Q., Liou, Y.-C., Ricci, A., Ferraguti, F., Lien, C., & Capogna, M. (2022) · Cell Reports · doi:10.1016/j.celrep.2024.114468 · Cited by 8 · see citing works
Lee, J., An, B., & Choi, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-90530-x · Cited by 7 · 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
- Authors
- Goosens, K. A., Hobin, J. A., & Maren, S.
- Affiliations
- University of Michigan (US)
- Corresponding author
- Maren, Stephen
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2003-12
- Volume
- 40
- Issue
- 5
- Pages
- 1013-1022
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2003951007
- Cited by
- 135
- References
- 53
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2023: 2 · 2022: 6 · 2021: 8 · 2020: 2 · 2019: 3 · 2018: 7 · 2017: 9 · 2016: 5 · 2015: 7 · 2014: 7 · 2013: 9 · 2012: 6
- FWCI
- 3.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 3516 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH065961, R29MH57865)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- lateral amygdala, fear conditioning, fear memory, associative learning, fear expression
- MeSH terms
- Action Potentials, Amygdala, Animals, Conditioning, Classical, Evoked Potentials, Auditory, Fear, Male, Neuronal Plasticity, Rats, Long-Evans, Rats
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