Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus
Abstract
Fear-arousing stimuli elicit innate reactions and can reinforce acquisition of new responses. We tested whether mechanisms mediating these conditioned stimulus (CS) properties were isomorphic or dissociable within the amygdala. Rats trained on a fear-conditioning task (CS paired with footshock) were then trained on an escape-from-fear task (EFF) in which the CS reinforced a locomotor response terminating the CS. Lateral nucleus (LA) lesions blocked acquisition of both conditioned freezing responses and the CS's reinforcement of a new response in the EFF task. Central nucleus (CE) lesions blocked conditioned freezing but not the EFF, whereas basal nucleus (B) lesions blocked the EFF but not conditioned freezing. Thus, activation of the LA by a CS seems to trigger conditioned reactions via CE and conditioned aversion via B activation, reduction of which reinforces new actions.
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?
In rats conditioned to a trauma-like fear response, if allowed to complete an escape response, the fear conditioning immediately disappeared.
“Tellingly, Ledoux found that in rats conditioned through such a procedure to a trauma-like fear response, if they were placed in the same experimental situation and allowed to complete an escape response, the fear conditioning immediately disappeared (Amorapanth et al., 2000).”
From Somatic experiencing: using interoception and proprioception as core elements of trauma therapy (2015) · cites this paper as Amorapanth et al., 2000
The lateral nucleus projects to the basal nucleus of the amygdala, which projects to the striatum, and these connections are essential for avoidance learning.
“The lateral nucleus also projects to the basal nucleus of the amygdala, which projects to the striatum. These connections are essential for avoidance learning (Amorapanth et al., 2000; Ramirez et al., 2015).”
From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Amorapanth et al., 2000
Instrumental control over threat involves the amygdala, striatum, and ventromedial prefrontal cortex in rodents.
“Instrumental control over threat has been shown to involve the amygdala, striatum, and ventromedial prefrontal cortex (vmPFC) in rodents.”
From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Amorapanth et al., 2000
The basal nucleus of the amygdala is engaged during avoidance learning and may transfer information about CS-US association to the striatum.
“However, the basal nucleus of the amygdala is engaged during avoidance learning and may transfer information about CS-US association to the striatum (Amorapanth et al., 2000; Ramirez et al., 2015).”
From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Amorapanth et al., 2000
Cites
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Self-citationPitkänen, A., Savander, V., & LeDoux, J. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01125-9 · Cited by 980 · see citing works
Self-citationAmygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit
Kapp, B. S., Frysinger, R. C., Gallagher, M., & Haselton, J. R. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90304-4 · Cited by 590 · see citing works
Miller, N. E. (1948) · Journal of Experimental Psychology · doi:10.1037/h0058455 · Cited by 537 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · see citing works
Self-citationThe 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 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
Uncertainty and anticipation in anxiety: an integrated neurobiological and psychological perspective
Grupe, D. W., & Nitschke, J. B. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3524 · Cited by 2,007 · see citing works
The Amygdaloid Complex: Anatomy and Physiology
SAH, P., FABER, E. S. L., LOPEZ DE ARMENTIA, M., & POWER, J. (2003) · Physiological Reviews · doi:10.1152/physrev.00002.2003 · Cited by 1,745 · see citing works
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
The role of ventromedial prefrontal cortex in the recovery of extinguished fear
Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06225.2000 · Cited by 957 · 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
LeDoux, J. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400335111 · Cited by 891 · see citing works
Self-citationNew 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 · see citing works
Self-citationAmygdala Microcircuits Controlling Learned Fear
Duvarci, S., & Pare, D. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.042 · Cited by 751 · see citing works
The Neuroscience of Mammalian Associative Learning
Fanselow, M. S., & Poulos, A. M. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070213 · Cited by 683 · see citing works
Parallel incentive processing: an integrated view of amygdala function
Balleine, B. W., & Killcross, S. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.03.002 · Cited by 622 · 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
Self-citationWilensky, A. E., Schafe, G. E., Kristensen, M. P., & LeDoux, J. E. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4316-06.2006 · Cited by 533 · see citing works
Self-citationAdolphs, R. (2013) · Current Biology · doi:10.1016/j.cub.2012.11.055 · Cited by 524 · see citing works
Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective
Schafe, G. E., Nader, K., Blair, H. T., & LeDoux, J. E. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01969-x · Cited by 510 · see citing works
Self-citationRelapse to cocaine-seeking after hippocampal theta burst stimulation
Vorel, S. R., Liu, X., Hayes, R. J., Spector, J. A., & Gardner, E. L. (2001) · Science · doi:10.1126/science.1058043 · Cited by 486 · see citing works
Goosens, K. A., & Maren, S. (2001) · Learning & Memory · doi:10.1101/lm.37601 · Cited by 451 · see citing works
Emotion, motivation, and the brain: Reflex foundations in animal and human research
Lang, P. J., & Davis, M. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)56001-7 · Cited by 410 · see citing works
The birth, death and resurrection of avoidance: a reconceptualization of a troubled paradigm
LeDoux, J. E., Moscarello, J., Sears, R., & Campese, V (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.166 · Cited by 348 · see citing works
Self-citationHall, J., Parkinson, J. A., Connor, T. M., Dickinson, A., & Everitt, B. J. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01577.x · Cited by 355 · see citing works
Somatic experiencing: using interoception and proprioception as core elements of trauma therapy
Payne, P., Levine, P. A., & Crane-Godreau, M. A. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00093 · Cited by 344 · see citing works
“Tellingly, Ledoux found that in rats conditioned through such a procedure to a trauma-like fear response, if they were placed in the same experimental situation and allowed to complete an escape response, the fear conditioning immediately disappeared (Amorapanth et al., 2000).”
BackgroundThe role of the striatum in aversive learning and aversive prediction errors
Delgado, M. R., Li, J., Schiller, D., & Phelps, E. A. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0161 · Cited by 328 · see citing works
Myers, B., McKlveen, J. M., & Herman, J. P. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.12.003 · Cited by 318 · see citing works
Overlapping neural systems mediating extinction, reversal and regulation of fear
Schiller, D., & Delgado, M. R. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.04.002 · Cited by 294 · see citing works
Amygdala–prefrontal dissociation of subliminal and supraliminal fear
Williams, L. M., Liddell, B. J., Kemp, A. H., Bryant, R. A., Meares, R. A., Peduto, A. S., & Gordon, E. (2006) · Human Brain Mapping · doi:10.1002/hbm.20208 · Cited by 257 · see citing works
Doux, L. (2012) · doi:10.1016/b978-0-444-53860-4.00021-0 · Cited by 241 · see citing works
A call to action: overcoming anxiety through active coping.
LeDoux, J. E., & Gorman, J. M. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.12.1953 · Cited by 238 · see citing works
Self-citationLesions of the Basal Amygdala Block Expression of Conditioned Fear But Not Extinction
Anglada-Figueroa, D., & Quirk, G. J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2600-05.2005 · Cited by 238 · see citing works
Neural structures mediating expression and extinction of platform-mediated avoidance
Bravo-Rivera, C., Roman-Ortiz, C., Brignoni-Perez, E., Sotres-Bayon, F., & Quirk, G. J. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0191-14.2014 · Cited by 206 · see citing works
Rosen, J. B. (2004) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582304265945 · Cited by 219 · see citing works
Hardt, O., Einarsson, E. Ö., & Nader, K. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100455 · Cited by 211 · see citing works
Self-citationActive Avoidance Requires a Serial Basal Amygdala to Nucleus Accumbens Shell Circuit
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
Self-citationAmygdala microcircuits mediating fear expression and extinction
Pare, D., & Duvarci, S. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.02.014 · Cited by 193 · see citing works
Waddell, J., Morris, R. W., & Bouton, M. E. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.2.324 · Cited by 183 · see citing works
The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats.
Choi, J.-S., Cain, C. K., & LeDoux, J. E. (2010) · Learning & Memory · doi:10.1101/lm.1676610 · Cited by 187 · see citing works
Self-citationKoo, J. W., Han, J.-S., & Kim, J. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1644-04.2004 · Cited by 179 · see citing works
A model of differential amygdala activation in psychopathy
Moul, C., Killcross, S., & Dadds, M. R. (2012) · Psychological Review · doi:10.1037/a0029342 · Cited by 159 · see citing works
Prepulse inhibition deficits in patients with panic disorder
Ludewig, S., Ludewig, K., Geyer, M. A., Hell, D., & Vollenweider, F. X. (2002) · Depression and Anxiety · doi:10.1002/da.10026 · Cited by 157 · see citing works
Trauma associated sleep disorder: a parasomnia induced by trauma
Mysliwiec, V., Brock, M. S., Creamer, J. L., O'Reilly, B. M., Germain, A., & Roth, B. J. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.01.004 · Cited by 150 · see citing works
Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding
Boeke, E. A., Moscarello, J. M., LeDoux, J. E., Phelps, E. A., & Hartley, C. A. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3261-16.2017 · Cited by 131 · see citing works
“These connections are essential for avoidance learning (Amorapanth et al., 2000; Ramirez et al., 2015).”
BackgroundInfluentialSelf-citationGlover, E. M., Phifer, J. E., Crain, D. F., Norrholm, S. D., Davis, M., Bradley, B., Ressler, K. J., & Jovanovic, T. (2011) · Depression and Anxiety · doi:10.1002/da.20880 · Cited by 130 · see citing works
Speed dependent descending control of freezing behavior in Drosophila melanogaster
Zacarias, R., Namiki, S., Card, G. M., Vasconcelos, M. L., & Moita, M. A. (2018) · Nature Communications · doi:10.1038/s41467-018-05875-1 · Cited by 106 · see citing works
Stressor controllability modulates fear extinction in humans
Hartley, C. A., Gorun, A., Reddan, M. C., Ramirez, F., & Phelps, E. A. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.003 · Cited by 110 · see citing works
An intra-amygdala circuit specifically regulates social fear learning
Twining, R. C., Vantrease, J. E., Love, S., Padival, M., & Rosenkranz, J. A. (2017) · Nature Neuroscience · doi:10.1038/nn.4481 · Cited by 93 · see citing works
Phasic activation of locus ceruleus neurons by the central nucleus of the amygdala
Bouret, S., Duvel, A., Onat, S., & Sara, S. J. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03491.2003 · Cited by 84 · see citing works
Cain, C. K., & LeDoux, J. E. (2007) · Journal of Experimental Psychology: Animal Behavior Processes · doi:10.1037/0097-7403.33.4.451 · Cited by 72 · see citing works
Self-citationCholinergic activation of the basolateral amygdala regulates unlearned freezing behavior in rats
Power, A. E., & McGaugh, J. L. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00046-3 · Cited by 65 · see citing works
Taking Action in the Face of Threat: Neural Synchronization Predicts Adaptive Coping
Collins, K. A., Mendelsohn, A., Cain, C. K., & Schiller, D. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.2152-14.2014 · Cited by 61 · see citing works
Hurlemann, R., Rehme, A. K., Diessel, M., Kukolja, J., Maier, W., Walter, H., & Cohen, M. X. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.04.004 · Cited by 51 · see citing works
Decision making in avoidance–reward conflict: a paradigm for non-human primates and humans
Sierra-Mercado, D., Deckersbach, T., Arulpragasam, A. R., Chou, T., Rodman, A. M., Duffy, A., McDonald, E. J., Eckhardt, C. A., Corse, A. K., Kaur, N., et al. (2015) · Brain Structure and Function · doi:10.1007/s00429-014-0796-7 · Cited by 44 · see citing works
Neural substrates of cognitive emotion regulation: a brief review
Öner, S. (2018) · Psychiatry and Clinical Psychopharmacology · doi:10.1080/24750573.2017.1407563 · Cited by 20 · see citing works
Kim, N., Kim, H. J., Hwang, J., Yoon, S. J., Cho, H. B., Renshaw, P. F., Lyoo, I. K., & Kim, J. E. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2010.11.005 · Cited by 11 · see citing works
- Authors
- Amorapanth, P., LeDoux, J. E., & Nader, K.
- Affiliations
- New York University (US)
- Corresponding author
- Nader, K.
- Venue
- Nature Neuroscience
- Published
- 2000-01
- Volume
- 3
- Issue
- 1
- Pages
- 74-79
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W1562182300
- Cited by
- 374
- References
- 4
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 9 · 2023: 7 · 2022: 8 · 2021: 6 · 2020: 10 · 2019: 10 · 2018: 14 · 2017: 12 · 2016: 14 · 2015: 14 · 2014: 17 · 2013: 22 · 2012: 15
- FWCI
- 12.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k02mh000956-07)
- National Institute of Mental Health (MH 46516, K02-MH00956, R37MH038774, R01MH046516)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- lateral amygdala, central amygdala, basal amygdala, fear conditioning, conditioned freezing, conditioned aversion, footshock, amygdala lesions, conditioned response acquisition, locomotor response
- MeSH terms
- Amygdala, Animals, Behavior, Animal, Conditioning, Classical, Conditioning, Operant, Electrodes, Implanted, Electrolysis, Electroshock, Fear, Models, Neurological, Stereotaxic Techniques, Rats, Sprague-Dawley, Rats
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