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Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction
Open accessAbstract
Recent studies implicate the hippocampus in contextual memory retrieval. The present experiments explore this possibility by examining the impact of reversible inactivation of the dorsal hippocampus (DH) on the context-specific expression of extinction. In experiment 1, rats were conditioned to fear a tone conditional stimulus (CS) and subsequently extinguished either in the same context as conditioning or in a novel context. A third group of rats underwent fear conditioning but did not receive extinction. After extinction, conditional fear to the tone CS was assessed in the conditioning context by measuring freezing. Rats extinguished in the conditioning context exhibited low levels of freezing, whereas those extinguished in a different context and those that received no extinction showed high levels of freezing. This indicates that the expression of extinction is context-specific. In experiment 2, the context-specific expression of extinction was disrupted by infusion of muscimol, a GABA(A) receptor agonist, into the DH. Rats that received muscimol infusions into the DH showed little freezing to the tone CS, regardless of whether the CS had been extinguished in the testing context or another context. In experiment 3, intrahippocampal muscimol infusions did not disrupt the expression of conditional freezing to the tone CS in rats that did not receive extinction. Thus, muscimol infusion into the DH produced a selective impairment in the context-specific expression of extinction. These results extend findings from other behavioral paradigms and provide additional support for a role for the hippocampus in contextual memory retrieval.
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“Reversible inactivation of the dorsal hippocampus, through either pharmacologic or chemogenetic means, interferes with context-specific information of a threat memory [40, 41].”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [40]
In the citing paper
“Also consistent with animal models (e.g., [40]), research suggests that the hippocampus is involved in contextual modulation of extinction and works in concert with the PFC during contextual extinction learning.”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [40]
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Understanding the dynamic and destiny of memories
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“acquisition and retrieval of extinction for both context-dependent fear-associated memories (Bernier et al., 2017; Corcoran et al., 2005; Corcoran and Maren, 2001; Hobin et al., 2006) and reward-associated memories (Bossert and Stern, 2014; Busse and Schwarting, 2016;”
BackgroundThe prelimbic cortex is critical for context-dependent fear expression
Kim, E. J., Kim, N., Kim, H. T., & Choi, J.-S. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00073 · Cited by 37
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“Additionally, greater hippocampal activation was observed in the renewal as compared to extinction group, lending further support to the importance of hippocampus in fear renewal (Corcoran and Maren, 2001, Corcoran and Maren, 2004, Corcoran et al., 2005, Ji and Maren, 2005).”
BackgroundResultPharmacological enhancement of drug cue extinction learning: translational challenges
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Mushroom Body Extrinsic Neurons in the Honeybee Brain Encode Cues and Contexts Differently
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“It appears that contextdependent learning requires an intact hippocampus (Chen et al., 1996; Logue et al., 1997; Holland and Bouton, 1999; Anagnostaras et al., 2001; Corcoran and Maren, 2001), whereas cued learning does not require the hippocampus (Gould et al.”
BackgroundRole of the basolateral amygdala and NMDA receptors in higher-order conditioned fear
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“Specifi cally, the hippocampus is thought to process contextual information during fear conditioning, extinction, and renewal (Wilson et al. , 1995 ; Frohardt et al. , 2000 ; Corcoran and Maren , 2001, 2004 ; Ji and Maren , 2005 ; Bouton et al. , 2006 ; Hobin et al. , 2006 ).”
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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 33
“This phenomenon also demonstrates that cued learning does not occur in isolation from contextual learning, although paradigms can be arranged to tease apart these components (LeDoux, 2000; Maren, 2001).”
InfluentialNeuronal Ensembles Organize Activity to Generate Contextual Memory
Marks, W. D., Yokose, J., 北村, 貴., & Ogawa, S. K. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.805132 · Cited by 27
Enhanced Histone Acetylation in the Infralimbic Prefrontal Cortex is Associated with Fear Extinction
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“While this literature points to the amygdala ([14]; for a review see [15]) and ventromedial prefrontal cortex [16] as being involved in extinction, Maren and colleagues [17,26,18] have also found that the dorsal hippocampus (DH) is especially important in the contextual control of extinction.”
BackgroundEvidence of a role for multiple memory systems in behavioral extinction.
Gabriele, A., & Packard, M. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.12.004 · Cited by 25
Ramirez, D. R., Buzzetti, R. A., & Savage, L. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.06.005 · Cited by 25
The transition from memory retrieval to extinction
Cammarota, M., Barros, D. M., Vianna, M. R. M. R., Bevilaqua, L. R., Coitinho, A. S., Szapiro, G., Izquierdo, L. A., Medina, J. H., & Izquierdo, I. (2004) · Anais da Academia Brasileira de Ciências · doi:10.1590/s0001-37652004000300011 · Cited by 28
“Retrieval has been traditionally considered to depend on the hippocampus (Eldridge et al. 2000, Corcoran and Maren 2001, *Member of Academia Brasileira de Ciências Correspondence to: Dr. Iván Izquierdo E-mail: izquier@terra.com.br Anderson et al. 2004).”
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Heldt, S. A., Coover, G. D., & Falls, W. (2002) · Hippocampus · doi:10.1002/hipo.10033 · Cited by 25
“However, Corcoran and Maren (2001) have recently demonstrated that reversible lesions of the dorsal hippocampus after training by infusion of muscimol, a GABAa receptor agonist, severely reduces the expression of fear outside the extinction context.”
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Yau, J. O.-Y., & McNally, G. P. (2018) · Journal of Experimental Psychology Animal Learning and Cognition · doi:10.1037/xan0000181 · Cited by 35
Neural correlates of fear appeal in advertising: An fMRI analysis
Mostafa, M. M. (2018) · Journal of Marketing Communications · doi:10.1080/13527266.2018.1497680 · Cited by 29
“For example, the hippocampus was implicated in emotional cue acquisition and retrieval (Corcoran and Maren 2001; Kalisch et al. 2006) and in contingency encoding (Cacciaglia et al. 2014).”
BackgroundNeural measures associated with configural threat acquisition
Stout, D. M., Glenn, D. E., Acheson, D. T., Spadoni, A. D., Risbrough, V. B., & Simmons, A. N. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.012 · Cited by 26
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Laurent, V., Chieng, B., & Balleine, B. (2016) · Current Biology · doi:10.1016/j.cub.2016.09.021 · Cited by 23
Early adversity disrupts the adult use of aversive prediction errors to reduce fear in uncertainty
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“Specifically,muscimol inactivation of the dorsal hippocampus reduces the rate of extinction and prevents the context dependency of extinction [50,53].”
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“Aside from mono-modal sensory cortical structures, the regulatory interplay between the amygdala and orbitofrontal (OFC) cortex has been demonstrated to account for, above all, time-delayed stimulus conditioning and devaluation conditioning (see Cardinal, Parkinson, Hall and Everitt 2002; Balleine, Kilcross and Dickin…”
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“…to be critically involved in the acquisition or retrieval of contextual fear memory and context-specific fear expression without affecting contextual discrimination or performance of the freezing response (Corcoran & Maren, 2001; Holt & Maren, 1999; Matus-Amat, Higgins, Barrientos, & Rudy, 2004).”
The Dorsal Subiculum Mediates the Acquisition of Conditioned Reinstatement of Cocaine-Seeking
Martin-Fardon, R., Ciccocioppo, R., Aujla, H., & Weiss, F. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301589 · Cited by 22
“…of the association between cocaine and the drugrelated context is consistent with literature showing that the hippocampus is a critical substrate for contextual memory (eg Corcoran and Maren, 2001; Holland and Bouton, 1999; Ji and Maren, 2007; Nadel et al, 1985; Phillips and LeDoux, 1992, 1994).”
ResultHao, S., Wang, Q., Tang, B., Wu, Z.-Y., Yang, T.-T., & Tang, J.-R. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1010-21.2021 · Cited by 21
“Freezing, defined as an absence of all movement except for respiration (Maren et al., 1994), was scored only if the animal was immobile for at least 1 s (Corcoran and Maren, 2001).”
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BackgroundMemory retrieval and its lasting consequences
Izquierdo, I., Vianna, M. R. M. R., Izquierdo, L. A., Barros, D. M., Szapiro, G., Coitinho, A. S., Muller, L., Cammarota, M., Bevilaqua, L. R., & Medina, J. H. (2002) · Neurotoxicity Research · doi:10.1080/10298420290031441 · Cited by 27
“, 2000) and extinction (Corcoran and Maren, 2001) are processed by the hippocampus.”
InfluentialA systems-neuroscience model of phasic dopamine.
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“Further, inactivating hippocampus with muscimol before extinction also produced a lack of either ABC or AAB renewal (Corcoran & Maren, 2001, 2004; Corcoran et al., 2005).”
Hsieh, H.-T., & Chang, C. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107170 · Cited by 20
Neural circuits involved in the renewal of extinguished fear
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“These findings suggest a role for the dorsal hippocampus in the context-dependent renewal of extinguished fear memories (30).”
BackgroundMethodNicotine-Derived Compounds as Therapeutic Tools Against Post-Traumatic Stress Disorder
Barreto, G. E., Yarkov, A., Ávila-Rodriguez, M., Aliev, G., & Echeverrı́a, V. (2015) · Current Pharmaceutical Design · doi:10.2174/1381612821666150710145250 · Cited by 23
“In fact, lesions of the hippocampus greatly affect the contextdependence of extinction in rodents [32, 33].”
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Genes and neurons: molecular insights to fear and anxiety
Stoppel, C. M., Albrecht, A., Pape, H., & Stork, O. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00229.x · Cited by 21
“Moreover, fear memory extinction is context-specific, and inactiva- tion of the dorsal hippocampus disrupts (cued) fear mem- ory extinction in a context-specific manner (Corcoran & Maren 2001).”
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“The HIP is involved in contextual representation and reports indicate that alteration in the context between extinction and testing affects the conditioning fear [50,51].”
Gao, M., Lengersdorf, D., Stüttgen, M. C., & Güntürkün, O. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.01.026 · Cited by 18
A Key Role for Nectin-1 in the Ventral Hippocampus in Contextual Fear Memory
Fantin, M., van der Kooij, M. A., Grosse, J., Krummenacher, C., & Sandi, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056897 · Cited by 19
“Importantly, while the amygdala is also involved in unimodal conditioning, such as auditory cue-shock associations, the role of the hippocampus has been associated with multimodal context-shock associations [15,16,17].”
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“Pre-training and post-training DH lesions, as well as pharmacological DH inactivation, have been shown to impair the context-specificity of fear extinction by reducing renewal (Corcoran & Maren, 2001; Ji & Maren, 2005).”
BackgroundCharacterizing the neural circuitry associated with configural threat learning
Stout, D. M., Glenn, D. E., Acheson, D. T., Simmons, A. N., & Risbrough, V. B. (2019) · Brain Research · doi:10.1016/j.brainres.2019.06.003 · Cited by 22
“Consistent with this, disrupting hippocampal activity via lesion and optogenetic manipulations is associated with reduced configural threat learning and contextual memory retrieval (Anagnostaras et al., 2001; Corcoran and Maren, 2001; Kheirbek et al., 2013).”
BackgroundPrasad, A. A., & McNally, G. P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110385 · Cited by 17
Graham, B. M., & Richardson, R. (2010) · Behavioral Neuroscience · doi:10.1037/a0019582 · Cited by 18
CA1‐specific deletion of NMDA receptors induces abnormal renewal of a learned fear response
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“In other words, the dorsal hippocampus is required for contextual gating; the cued fear response is supressed in both a context in which it was extinguished as well as a novel context (Corcoran and Maren, 2001; Ji and Maren, 2005; Ji and Maren, 2008).”
BackgroundInfluentialExtinction learning is slower, weaker and less context specific after alcohol
Bisby, J., King, J., Sulpizio, V., Dégeilh, F., Curran, H., & Burgess, N. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.07.014 · Cited by 17
“At retrieval, context dictates whether an extinction memory successfully competes with the fear memory (Alvarez, Johnson, & Grillon, 2007; Bouton & King, 1983; Corcoran & Maren, 2001).”
Nordquist, R., Pennartz, C., Uylings, H., Joosten, R., Jonker, A., Groenewegen, H., & Voorn, P. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.014 · Cited by 17
Fear Conditioning and Extinction
Graham, B. M., & Milad, M. R. (2016) · Innovations in cognitive neuroscience · doi:10.1007/978-1-4614-3846-5_8 · Cited by 2
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“The septum and the hippocampus are key components of the behavioral inhibition system regulating emotional behavior and cognitive functions, especially learning and memory, and the septohippocampal circuits are important for fear-related behaviors [42,43].”
BackgroundInput associativity underlies fear memory renewal
Li, W., Wu, Y., Gu, X., Fan, H.-R., Wang, Q., Zhu, J., Yi, X., Wang, Q., Jiang, Q., Li, Y., et al. (2021) · National Science Review · doi:10.1093/nsr/nwab004 · Cited by 17
“It has long been considered that this contextual control of extinguished fear memory critically depends on the hippocampus, as pharmacological inhibition of either the dorsal [30] or ventral [32] areas of this structure leads to a context-independent expression of extinction andprevents fear renewal.”
Dorsal hippocampus plays a causal role in context-induced reinstatement of alcohol-seeking in rats.
Felipe, J., Palombo, P., Bianchi, P., Zaniboni, C. R., Anesio, A., Yokoyama, T., Engi, S. A., Carneiro-de-Oliveira, P. E., Planeta, C. D. S., Leão, R. M., et al. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112978 · Cited by 16
Decreased plasma adiponectin among male firefighters with symptoms of post-traumatic stress disorder
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“…particular brain regions showed that local hippocampal GABA A agonism in rats disrupted contextual fear extinction learning (Corcoran et al. 2005; Corcoran and Maren 2001), a result that closely corresponds to our finding of reduced hippocampal activation associated with impaired extinction…”
InfluentialLiu, B.-G., Dobretsov, M., Stimers, J., & Zhang, J.-M. (2008) · The Open Pain Journal · doi:10.2174/1876386300902010001 · Cited by 16
“Traditionally, retrieval has been related to the hippocampus [64-66].”
BackgroundClosed-loop brain stimulation augments fear extinction in male rats
Sierra, R. O., Pedraza, L. K., Barcsai, L., Pejin, A., Li, Q., Kozák, G., Takeuchi, Y., Nagy, A. J., Lörincz, M. L., Devinsky, O., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39546-7 · Cited by 16
“Furthermore, inactivation of the hippocampus has been found to enhance extinction to the CS+ and promote low fear expression in environments different from the extinction context 18,19 .”
BackgroundSingh, S. P., Siddiqui, S. A., Tripathy, S., Kumar, S., Saha, S., Ugale, R. R., Modi, D. R., & Prakash, A. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.06.004 · Cited by 14
Kappa opioid receptors mediate where fear is expressed following extinction training.Preprint
Cole, S., Richardson, R., & McNally, G. (2011) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.2049511 · Cited by 15
“There is some evidence that the hippocampus is important for renewal of fear because lesions or temporary inactivation of the dorsal hippocampus (DH) prevent renewal (Corcoran and Maren 2001, 2004; Ji and Maren 2005).”
BackgroundCued Fear Conditioning in Carioca High- and Low-Conditioned Freezing Rats
Macêdo-Souza, C., Maisonnette, S. S., Filgueiras, C. C., Landeira-Fernández, J., & Krahe, T. E. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00285 · Cited by 18
Efficacy and mechanisms of non-invasive brain stimulation to enhance exposure therapy: A review
Nuñez, M. C., Zinbarg, R. E., & Mittal, V. A. (2019) · Clinical Psychology Review · doi:10.1016/j.cpr.2019.04.001 · Cited by 15
Todd, T. P., Jiang, M. Y., DeAngeli, N. E., & Bucci, D. J. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.11.033 · Cited by 14
Fu, J., Xing, X., Han, M., Xu, N., Piao, C.-J., Zhang, Y., & Zheng, X.-G. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.12.006 · Cited by 14
Increased hippocampal volume and gene expression following cognitive behavioral therapy in PTSD
Moustafa, A. A. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00747 · Cited by 13
“Further, many animal and human studies show that the hippocampus is involved in contextual fear responses (Anagnostaras et al., 1999; Corcoran and Maren, 2001; Ji and Maren, 2007; Acheson et al., 2012), such that hippocampal damage leads to increased fear response regardless of the context. fMRI…”
BackgroundContext Processing in Aging: Older Mice Are Impaired in Renewal of Extinguished Fear
Sanders, M. J. (2011) · Experimental Aging Research · doi:10.1080/0361073x.2011.619874 · Cited by 14
“After a 3-min exposure period, they were exposed to a single tone of 8-min duration (modeled after Corcoran & Maren, 2001).”
BackgroundMethodInfluentialRǎdulescu, A., & Mujica-Parodi, L. R. (2009) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2009.04.017 · Cited by 13
“Conversely, however, studies such as that of Corcoran and Maren (2001) have opened the possibility that hippocampal projections to the B might be important for contextual contributions in fear extinction.”
ResultDelamater, A. R., Campese, V. D., & Westbrook, R. F. (2009) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/a0013293 · Cited by 15
Extract of Ginkgo biloba EGb 761 facilitates fear conditioning measured by fear-potentiated startle.
Yang, Y.-L., Su, Y., Ng, M.-C., Chang, C.-L., & Lu, K.-T. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.04.003 · Cited by 14
Docosahexaenoic Acid Helps to Lessen Extinction Memory in Rats
Hashimoto, M., Hossain, S., Katakura, M., al Mamun, A., & Shido, O. (2018) · Molecules · doi:10.3390/molecules23020451 · Cited by 13
“Memory consolidation and extinction of conditioned fear may be dependent on NMDAR activities in the hippocampus [55,56].”
BackgroundAhnaou, A., Raeyemaekers, L., Huysmans, H., & Drinkenburg, W. H. I. M. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.035 · Cited by 16
Schizophrenia--a parameters' game?
Rǎdulescu, A. R. (2007) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2008.05.009 · Cited by 13
“Conversely however, some studies ( Corcoran and Maren, 2001 ) have opened the possibility that hippocampal projections to the B might be important for contextual contributions in fear extinction.”
Hiraide, S., Saito, Y., Matsumoto, M., Yanagawa, Y., Ishikawa, S., Kubo, Y., Inoue, S., Yoshioka, M., & Togashi, H. (2012) · Journal of Pharmacological Sciences · doi:10.1254/jphs.12023fp · Cited by 13
Urcelay, G., & Miller, R. R. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21004-3 · Cited by 13
Namkung, H., Thomas, K. L., Hall, J., & Sawa, A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.12.025 · Cited by 17
Wang, H., Xing, X., Liang, J., Bai, Y.-J., Lui, Z., & Zheng, X.-G. (2014) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2014.06.003 · Cited by 12
“Lastly, after extinction, the hippocampus, which serves as a key structure of glucocorticoid action in the brain, is critical for fear renewal (Corcoran and Maren, 2001, 2004; Ji and Maren, 2005, 2007).”
Campese, V. D., & Delamater, A. R. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.04.014 · Cited by 10
Fujiwara, H., Sawa, K., Takahashi, M., Lauwereyns, J., Tsukada, M., & Aihara, T. (2012) · Cognitive Neurodynamics · doi:10.1007/s11571-012-9208-y · Cited by 12
Hamlin, A., Blatchford, K., & McNally, G. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.07.035 · Cited by 12
“Bouton, 2004; Corcoran and Maren, 2001, 2004; Frohardt et al., 2000).”
Early postnatal stress and neural circuit underlying emotional regulation.
Matsumoto, M., Yoshioka, M., & Togashi, H. (2009) · International review of neurobiology · doi:10.1016/s0074-7742(09)85007-1 · Cited by 12
“Several studies, however, have provided evidence that hippocampus-dependent extinction is involved in contextual encoding processes (Corcoran and Maren, 2001, 2004; Ji and Maren, 2005) and is mediated by protein synthesis-independent mechanisms (Fischer et al., 2004; Lattal and Abel, 2001).”
BackgroundZoicas, I., Mühle, C., Schumacher, F., Kleuser, B., & Kornhuber, J. (2023) · Cells · doi:10.3390/cells12101355 · Cited by 11
“Besides modulating emotional behavior and cognitive functions, the hippocampus regulates fear-related behaviors together with the prefrontal cortex, lateral septum and amygdala [54,55] and processes contextual information, i.”
BackgroundXue, L., Li, Z. D., Chen, Z. X., Wang, X. G., Shi, Y., & Zhao, H. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.014 · Cited by 11
“…memory (Kim and Fanselow, 1992; Phillips and LeDoux, 1992), numerous studies have implicated it in the contextual modulation of fear extinction (Corcoran and Maren, 2001, 2004; Corcoran et al., 2005), moreover, different subfields of the hippocampus had different contributions in extinction.”
MethodInfluentialCole, S., Richardson, R., & McNally, G. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058701 · Cited by 12
“In light of the prior studies demonstrating involvement of the DH in the renewal of fear [5,23], it might seem surprising that here infusion of norBNI into the DH had no significant effect.”
BackgroundInfluentialSepahvand, T., Power, K. D., Qin, T., & Yuan, Q. (2023) · Biology · doi:10.3390/biology12101274 · Cited by 17
“The role of hippocampus, which is reciprocally connected to the BLA [131], has been shown to play a role in threat extinction and renewal [132].”
Li, Y., Zhi, W., Qi, B., Wang, L., & Hu, X. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1216524 · Cited by 16
“For example, inactivating the HPC using pharmacological techniques impairs the renewal of extinguished memory (Corcoran and Maren, 2001; Ji and Maren, 2008).”
Method
Metadata
- Authors
- Corcoran, K. A., & Maren, S.
- Affiliations
- University of Michigan (US)
- ORCID
- Maren, Stephen
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-03-01
- Volume
- 21
- Issue
- 5
- Pages
- 1720-1726
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6762930
- OpenAlex
- W1525373779
- Cited by
- 455
- References
- 0
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 14 · 2023: 15 · 2022: 6 · 2021: 19 · 2020: 18 · 2019: 17 · 2018: 17 · 2017: 21 · 2016: 21 · 2015: 20 · 2014: 26 · 2013: 30 · 2012: 25
- FWCI
- 8.22
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- Funders
- National Institutes of Health (5r29mh057865-03)
- National Institute of Mental Health (MH57865)
- 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
- hippocampus, dorsal hippocampus, fear memory, fear extinction, muscimol, GABAA receptor, fear conditioning, freezing behavior, hippocampal inactivation
- MeSH terms
- Acoustic Stimulation, Animals, Behavior, Animal, Conditioning, Classical, Cues, Electroshock, Extinction, Psychological, Fear, Hippocampus, Infusions, Parenteral, Male, Memory, Microinjections, Muscimol, GABA Agonists, Rats, Long-Evans, Rats, GABA-A Receptor Agonists
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