Cited by 152Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

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Role of the Amygdala in Fear Extinction Measured with Potentiated Startle

DAVIS, MICHAEL, WALKER, DAVID L., MYERS, KARYN M.·2003·Annals of the New York Academy of Sciences

DOI 10.1111/j.1749-6632.2003.tb07084.x

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Abstract

A bstract: Although much is now known about the neural basis of excitatory fear conditioning, much less is known about the neural basis of inhibitory conditioning. One type of inhibitory conditioning is extinction, a process in which stimuli that elicit fear by virtue of previous associations with aversive stimuli such as shock (excitatory fear conditioning) are now presented in the absence of the aversive stimuli (extinction training). As a result, the ability of the conditioned stimulus to elicit fear gradually diminishes. Extinction is different from forgetting and does not reflect an erasure of the original fear memory. Instead, extinction is an active form of inhibitory learning that competes with excitatory fear conditioning. Infusions into the amygdala (a brain area essential for excitatory fear conditioning) of either NMDA receptor antagonists or inhibitors of the NMDA‐receptor‐linked mitogen‐activated protein kinase cascade block extinction learning. Conversely, the NMDA receptor agonist D‐cycloserine facilitates extinction after either systemic administration or intra‐amygdala infusion. Because therapeutic interventions based on extinction procedures are commonly used to treat fear disorders, and because D‐cycloserine is a widely available and safe compound, D‐cycloserine or similar agents might be usefully combined with traditional extinction‐based approaches in the treatment of clinical fear.

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Early extinction after fear conditioning yields a context-independent and short-term suppression of conditional freezing in rats.Preprint
Chang, C.-H., & Maren, S. (2009) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.1085009 · Cited by 65
“However, with repeated presentations of the CS-alone, the previously acquired CR gradually subsides, a process called extinction (Davis et al. 2003; Maren and Quirk 2004; Kim and Jung 2005; Myers and Davis 2007).”
Background
Neuropeptides at the crossroad of fear and hunger: a special focus on neuropeptide Y
Comeras, L. B., Herzog, H., & Tasan, R. O. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14179 · Cited by 72
Anatomy and aging of the amygdala and hippocampus in autism spectrum disorder: an in vivo magnetic resonance imaging study of Asperger syndrome
Murphy, C. M., Deeley, Q., Daly, E. M., Ecker, C., O'Brien, F. M., Hallahan, B., Loth, E., Toal, F., Reed, S., Hales, S., et al. (2012) · Autism Research · doi:10.1002/aur.227 · Cited by 63
“For example, the amygdala plays a central role in fear and anxiety [Davis et al., 2003; LeDoux, 2003]; people with an ASD have a significantly increased risk of experiencing stress and anxiety disorders [for review, see White, Oswald et al., 2009]; and stress in turn impacts on amygdala development…”
Background
The effects of cannabinoids on contextual conditioned fear in CB1 knockout and CD1 mice
Mikics, É., Dombi, T., Barsvári, B., Varga, B., Ledent, C., Freund, T., & Haller, J. (2006) · Behavioural Pharmacology · doi:10.1097/00008877-200605000-00003 · Cited by 61
“Moreover, the amygdala appears specifically involved in fear extinction as measured with potentiated startle (Davis et al., 2003).”
BackgroundMethod
A Central Amygdala-Substantia Innominata Neural Circuitry Encodes Aversive Reinforcement Signals
Cui, Y., Lv, G., Jin, S., Peng, J., Yuan, J., He, X., Gong, H., Xu, F., Xu, T., & Li, H. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.062 · Cited by 65
Memory as a new therapeutic target
Nader, K., Hardt, O. M., & Lanius, R. A. (2013) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2013.15.4/knader · Cited by 67
Dopamine D1 receptors co-distribute with N-methyl-D-aspartic acid type-1 subunits and modulate synaptically-evoked N-methyl-D-aspartic acid currents in rat basolateral amygdala.
Pickel, V., Colago, E. E., Mania, I., Molosh, A., & Rainnie, D. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.06.059 · Cited by 59
Differential abnormalities of functional connectivity of the amygdala and hippocampus in unipolar and bipolar affective disorders
Benson, B. E., Willis, M. W., Ketter, T. A., Speer, A., Kimbrell, T. A., Herscovitch, P., George, M. S., & Post, R. M. (2014) · Journal of Affective Disorders · doi:10.1016/j.jad.2014.05.045 · Cited by 47
“The amygdala has been closely linked to the modulation of conditioned fear and other conditioned emotional learning paradigms (LeDoux, 1996; Davis, 1995; Davis et al., 2003).”
Background
Strain difference in the effect of infralimbic cortex lesions on fear extinction in rats.
Chang, C., & Maren, S. (2010) · Behavioral Neuroscience · doi:10.1037/a0019479 · Cited by 63
Morphology and dendritic maturation of developing principal neurons in the rat basolateral amygdala
Ryan, S. J., Ehrlich, D., & Rainnie, D. G. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0939-x · Cited by 56
“The basolateral nucleus of the amygdala (BLA) is critical for the production of appropriate emotional responses and the processing of emotional memories (Davis et al. 2003; LeDoux 2007; Pape and Pare 2010; Stuber et al. 2011).”
Neural mechanisms of freezing and passive aversive behaviors
Jhou, T. (2005) · The Journal of comparative neurology · doi:10.1002/cne.20734 · Cited by 51
“Animals with amygdala lesions display marked impairments in freezing to cues previously associated with aversive outcomes (Pellegrino, 1968; Slotnick, 1973; LeDoux, 2000; Davis et al., 2003).”
Background
A review of the neural basis underlying the acoustic startle response with a focus on recent developments in mammals.
Zheng, A. X., & Schmid, S. (2023) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105129 · Cited by 49
Protein synthesis inhibitors, gene superinduction and memory: too little or too much protein?
Radulovic, J., & Tronson, N. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.08.008 · Cited by 49
Cortico-amygdala circuits: Role in the conditioned stress response
Berretta, S. (2005) · Stress · doi:10.1080/10253890500489395 · Cited by 49
“A new learning event, defined as extinction of fear conditioning, has to take place in order to inhibit the stress response to a CS that no longer predicts danger (Davis et al. 2003; Rescorla 2001).”
Background
Exposure therapy, D-cycloserine, and functional magnetic resonance imaging in patients with snake phobia: a randomized pilot study.
Nave, A. M., Tolin, D., & Stevens, M. (2012) · Journal of Clinical Psychiatry · doi:10.4088/jcp.11m07564 · Cited by 48
Posttraumatic stress disorder and traumatic stress: from bench to bedside, from war to disaster
Ursano, R. J., Goldenberg, M., Zhang, L., Carlton, J. R., Fullerton, C. S., Li, H., Johnson, L. R., & Benedek, D. M. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05721.x · Cited by 39
The entorhinal cortex plays a role in extinction
Bevilaqua, L. R., Bonini, J. S., Rossato, J. I., Izquierdo, L. A., Cammarota, M., & Izquierdo, I. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.10.001 · Cited by 49
Alterations in extracellular levels of gamma-aminobutyric acid in the rat basolateral amygdala and periaqueductal gray during conditioned fear, persistent pain and fear-conditioned analgesia.
Rea, K., Lang, Y., & Finn, D. (2009) · Journal of Pain · doi:10.1016/j.jpain.2009.04.019 · Cited by 46
The effect of acute or repeated stress on the corticotropin releasing factor system in the CRH-IRES-Cre mouse: A validation study.
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The CB1 Receptor as an Important Mediator of Hedonic Reward Processing
Friemel, C., Zimmer, A., & Schneider, M. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.86 · Cited by 43
“In particular, the fear-potentiated startle paradigm, the augmentation of the ASR in an aversive emotional state, has been used since then to investigate the pharmacological and neuronal basics of fear in both humans and rats (eg, Davis, 1998; Lang, 1995; Davis et al, 2003; Norrholm et al, 2006).”
Method
NMDA Partial Agonist Reverses Blocking of Extinction of Aversive Memory by GABAA Agonist in the Amygdala
Akirav, I. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301050 · Cited by 41
“This view is compatible with evidence that GABAA receptor agonists interrupt, whereas NMDA receptor agonists facilitate extinction of fear memories (Davis et al, 2003; Pereira et al, 1989; Santini et al, 2001; Walker et al, 2002).”
BackgroundInfluential
Pharmacological Findings on the Biochemical Bases of Memory Processes: A General View
Izquierdo, I., Cammarota, M., Medina, J. H., & Bevilaqua, L. R. (2004) · Neural Plasticity · doi:10.1155/np.2004.159 · Cited by 45
Developmental Epidemiology of PTSD
Koenen, K. C. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1364.020 · Cited by 57
Effects of the NMDA receptor antagonist memantine on the expression and development of acute opiate dependence as assessed by withdrawal-potentiated startle and hyperalgesia
Harris, A. C., Rothwell, P. E., & Gewirtz, J. C. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0998-2 · Cited by 36
“Given that startle is increased during states of fear and anxiety in both humans and animals (Lang et al. 2000; Davis et al. 2003), “withdrawal-potentiated startle” may reflect the anxiogenic effects of withdrawal.”
Cell-type-specific interrogation of CeA Drd2 neurons to identify targets for pharmacological modulation of fear extinction
McCullough, K. M., Daskalakis, N. P., Gafford, G. M., Morrison, F. G., & Ressler, K. J. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0190-y · Cited by 40
Modulation of conditioned fear, fear-conditioned analgesia, and brain regional c-Fos expression following administration of muscimol into the rat basolateral amygdala.
Rea, K., Roche, M., & Finn, D. (2011) · Journal of Pain · doi:10.1016/j.jpain.2010.12.010 · Cited by 37
Extinction and reacquisition of a fear-motivated memory require activity of the Src family of tyrosine kinases in the CA1 region of the hippocampus
BEVILAQUA, L., DASILVA, W., MEDINA, J., IZQUIERDO, I., & CAMMAROTA, M. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.03.005 · Cited by 35
Exposure to an obesogenic diet during adolescence leads to abnormal maturation of neural and behavioral substrates underpinning fear and anxiety
Vega-Torres, J. D., Haddad, E., Lee, J. B., Kalyan-Masih, P., Maldonado, W. I., Pérez, L. L., Vázquez, D. M. P., Torres, Y. A., Santiago, J. M., Obenaus, A., et al. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.01.011 · Cited by 33
An orchestrating role of mitochondria in the origin and development of post-traumatic stress disorder
Lushchak, O. V., Strilbytska, O. M., Koliada, A. K., & Storey, K. B. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2022.1094076 · Cited by 43
“For example, the amygdala lateral nucleus is known to play a central role in triggering fear (Davis et al., 2003; Morey et al., 2012).”
Background
The effects of midazolam and D-cycloserine on the release of glutamate and GABA in the basolateral amygdala of low and high anxiety rats during extinction trial of a conditioned fear test.
Lehner, M., Wisłowska-Stanek, A., Taracha, E., Maciejak, P., Szyndler, J., Skórzewska, A., Turzyńska, D., Sobolewska, A., Hamed, A., Bidziński, A., et al. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.08.014 · Cited by 33
Candidate genes for panic disorder: insight from human and mouse genetic studies
Gratacòs, M., Sahún, I., Gallego, X., Amador‐Arjona, A., Estivill, X., & Dierssen, M. (2007) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2007.00318.x · Cited by 33
“During normal functioning, the amygdala continuously compares incoming sensory stimuli with previously learned aversive stimuli (Davis et al. 2003; LeDoux 1996), leading to the activation of appropriate conditioned response pathways.”
Background
Differential effects of training intertrial interval on acquisition of trace and long-delay fear conditioning in rats.
Detert, J. A., Kampa, N. D., & Moyer, J. R. (2008) · Behavioral Neuroscience · doi:10.1037/a0013512 · Cited by 29
Appetitive odor-cue conditioning attenuates the acoustic startle response in rats.
Schneider, M., & Spanagel, R. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.12.017 · Cited by 31
Pharmacotherapy for performance anxiety disorders: occasionally useful but typically contraindicated.
Birk, L. (2004) · Journal of Clinical Psychology · doi:10.1002/jclp.20044 · Cited by 31
Early-Life Experiences: Enduring Behavioral, Neurological, and Endocrinological Consequences
Romeo, R. D., Tang, A. C., & Sullivan, R. M. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00062-0 · Cited by 25
Autismo: tratamentos psicofarmacológicos e áreas de interesse para desenvolvimentos futuros
Nikolov, R., Jonker, J., & Scahill, L. D. (2006) · Brazilian Journal of Psychiatry · doi:10.1590/s1516-44462006000500006 · Cited by 41
Organization of Neural Systems for Aversive Information Processing: Pain, Error, and Punishment
Kobayashi, S. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00136 · Cited by 32
“…escape, and freezing) to an innocuous stimulus (i.e., a tone) that predicts a noxious stimulus (i.e., electric shock), and amygdala lesions cause behavioral impairments in these aversive conditioning (Pellegrino, 1968; Slotnick, 1973; Wilensky et al., 1999; Davis et al., 2003; Blair et al., 2005).”
Background
Evidence for direct projections from the basal nucleus of the amygdala to retrosplenial cortex in the Macaque monkey
Buckwalter, J. A., Schumann, C. M., & Van Hoesen, G. W. (2008) · Experimental Brain Research · doi:10.1007/s00221-007-1203-x · Cited by 26
“There is an abundance of evidence from animal (LeDoux 2000; Davis et al. 2003; Bauman et al. 2004) and human (Adolphs et al. 1994; Adolphs et al. 1995; Whalen et al. 1998; Buchel and Dolan 2000; Whalen et al. 2004) studies to implicate the amygdala in emotional processing as well, particularly the…”
Background
Affective startle modulation and psychopathology: Implications for appetitive and defensive brain systems
Boecker, L., & Pauli, P. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.019 · Cited by 34
Opioid modulation of Fos protein expression and olfactory circuitry plays a pivotal role in what neonates remember.Preprint
Roth, T., Moriceau, S., & Sullivan, R. (2006) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.301206 · Cited by 22
“…hippocampus, frontal cortex, and amygdala, with the basolateral complex of the amygdala serving as a potential site for stimuli associations (LeDoux et al. 1990; Fendt and Fanselow 1999; Schafe et al. 2000; Maren 2001; Davis et al. 2003; Fanselow and Poulos 2005; Rudy and Matus-Amat 2005).”
Background
Effects of reinforcement schedule on facilitation of operant extinction by chlordiazepoxide.
Leslie, J., Shaw, D. R., Gregg, G., McCormick, N., Reynolds, D., & Dawson, G. (2005) · Journal of The Experimental Analysis of Behavior · doi:10.1901/jeab.2005.71-04 · Cited by 22
“Specific procedures used include conditioned freezing (Ledgerwood, Richardson, & Cranney, 2004) and the fear-potentiated startle ( Davis, Walker, & Myers, 2003 ).”
Method
Fear Conditioning in Rodents and Humans
Milad, M., Igoe, S. A., & Orr, S. (2011) · Neuromethods · doi:10.1007/978-1-60761-883-6_5 · Cited by 21
Neural circuits involved in the renewal of extinguished fear
Chen, W., Wang, Y., Wang, X., & Li, H. (2017) · IUBMB Life · doi:10.1002/iub.1636 · Cited by 22
Effect of Acute Swim Stress on Plasma Corticosterone and Brain Monoamine Levels in Bidirectionally Selected DxH Recombinant Inbred Mouse Strains Differing in Fear Recall and Extinction
Browne, C. A., Hanke, J., Rose, C., Walsh, I., Foley, T., Clarke, G., Schwegler, H., Cryan, J., & Yilmazer-Hanke, D. (2014) · Stress · doi:10.3109/10253890.2014.954104 · Cited by 20
“Fear extinction is the gradual weakening of this learned fear response upon repetitive presentations of the CS in the absence of the US (Davis et al., 2003; Sotres-Bayon et al., 2004).”
Background
Enhanced stress reactivity in nitric oxide synthase type 2 mutant mice: findings in support of astrocytic nitrosative modulation of behavior.
Abu-Ghanem, Y., Cohen, H., Buskila, Y., Grauer, E., & Amitai, Y. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.07.043 · Cited by 20
“The ASR is often associated with fear reactivity and is known to be enhanced by stress (Davis et al., 2003).”
Background
Post-natal treatment by a blood-brain-barrier permeable calpain inhibitor, SNJ1945 rescued defective function in lissencephaly
Toba, S., Tamura, Y., Kumamoto, K., Yamada, M., Takao, K., Hattori, S., Miyakawa, T., Kataoka, Y., Azuma, M., Hayasaka, K., et al. (2013) · Scientific Reports · doi:10.1038/srep01224 · Cited by 19
D-Cycloserine Augmentation of Cognitive-Behavioral Therapy: Directions for Pilot Research in Pediatric Obsessive-Compulsive Disorder
Storch, E. A., McKay, D., Reid, J. M., GELLER, D. A., Goodman, W. K., Lewin, A. B., & Murphy, T. K. (2010) · Child & Youth Care Forum · doi:10.1007/s10566-010-9094-6 · Cited by 15
“and memory (Davis 2000; Davis et al. 2003; Myers and Davis 2002).”
BackgroundInfluential

Authors: DAVIS, M., WALKER, D. L., & MYERS, K. M.
Affiliations: Emory University (US)
Corresponding author: DAVIS, MICHAEL
ORCID: WALKER, DAVID L.
Venue: Annals of the New York Academy of Sciences
Publisher: Wiley
Published: 2003-04
Volume: 985
Issue: 1
Pages: 218-232
ISSN: 0077-8923 (ISSN-L)
1749-6632
DOI: 10.1111/j.1749-6632.2003.tb07084.x
OpenAlex: W2154648089
Cited by: 152
References: 0
Citations by year: 2026: 2 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 2 · 2019: 3 · 2018: 6 · 2017: 7 · 2016: 3 · 2015: 3 · 2014: 9 · 2013: 9 · 2012: 5
FWCI: 1.73
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 1029 d)
Locations: Annals of the New York Academy of Sciences (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (MH59906, MH-57250, R01MH057250, P50MH052384, R01MH059906, P50MH058922, MH58922, MH 47840, MH-52384)
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: amygdala, fear extinction, inhibitory conditioning, NMDA receptor, D-cycloserine, mitogen-activated protein kinase, extinction learning, fear memory
MeSH terms: Amygdala, Animals, Extinction, Psychological, Fear, Reflex, Startle, Receptors, N-Methyl-D-Aspartate

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Role of the Amygdala in Fear Extinction Measured with Potentiated Startle

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