Pathway-Selective Adjustment of Prefrontal-Amygdala Transmission during Fear Encoding
Open accessAbstract
Conditioned fear requires neural activity in the basolateral amygdala (BLA) and medial prefrontal cortex (mPFC), structures that are densely interconnected at the synaptic level. Previous work has suggested that anatomical subdivisions of mPFC make distinct contributions to fear expression and inhibition, and that the functional output of this processing is relayed to the BLA complex. However, it remains unknown whether synaptic plasticity in mPFC-BLA networks contributes to fear memory encoding. Here we use optogenetics and ex vivo electrophysiology to reveal the impact of fear conditioning on BLA excitatory and feedforward inhibitory circuits formed by projections from infralimbic (IL) and prelimbic (PL) cortices. In naive mice, these pathways recruit equivalent excitation and feedforward inhibition in BLA principal neurons. However, fear learning leads to a selective decrease in inhibition:excitation balance in PL circuits that is attributable to a postsynaptic increase in AMPA receptor function. These data suggest a pathway-specific mechanism for fear memory encoding by adjustment of mPFC-BLA transmission. Upon reengagement of PL by conditioned cues, these modifications may serve to amplify emotional responses.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Following auditory fear conditioning, excitatory responses evoked by prelimbic cortical inputs in the BLA are increased as a result of enhanced AMPA-type glutamate receptor function.
“Following auditory fear conditioning, however, excitatory responses evoked by prelimbic cortical inputs in the BLA are increased as a result of enhanced AMPA-type glutamate receptor function113.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [113]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.2.274 · Cited by 3,262 · see citing works
Neurons in medial prefrontal cortex signal memory for fear extinction
Milad, M. R., & Quirk, G. J. (2002) · Nature · doi:10.1038/nature01138 · Cited by 1,836 · cited 1× · see citing works
“In contrast, IL activity is associated with fear inhibition (Milad and Quirk, 2002).”
BackgroundPhelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.042 · Cited by 1,753 · see citing works
Sesack, S. R., Deutch, A. Y., Roth, R. H., & Bunney, B. S. (1989) · Journal of Comparative Neurology · doi:10.1002/cne.902900205 · Cited by 1,568 · see citing works
The contextual brain: implications for fear conditioning, extinction and psychopathology
Maren, S., Phan, K. L., & Liberzon, I. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3492 · Cited by 1,547 · see citing works
Neurobiological Basis of Failure to Recall Extinction Memory in Posttraumatic Stress Disorder
Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., Zeidan, M. A., Handwerger, K., Orr, S. P., & Rauch, S. L. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.026 · Cited by 1,339 · see citing works
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
Sierra-Mercado, D., Padilla-Coreano, N., & Quirk, G. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.184 · Cited by 1,190 · see citing works
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
Engineering a memory with LTD and LTP
Nabavi, S., Fox, R., Proulx, C. D., Lin, J. Y., Tsien, R. Y., & Malinow, R. (2014) · Nature · doi:10.1038/nature13294 · Cited by 980 · see citing works
Extinction-Reconsolidation Boundaries: Key to Persistent Attenuation of Fear Memories
Monfils, M.-H., Cowansage, K. K., Klann, E., & LeDoux, J. E. (2009) · Science · doi:10.1126/science.1167975 · Cited by 960 · see citing works
Fear conditioning induces a lasting potentiation of synaptic currents in vitro
McKernan, M. G., & Shinnick-Gallagher, P. (1997) · Nature · doi:10.1038/37605 · Cited by 771 · see citing works
Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli
Lammel, S., Ion, D. I., Roeper, J., & Malenka, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.03.025 · Cited by 766 · see citing works
Synaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens
Britt, J. P., Benaliouad, F., McDevitt, R. A., Stuber, G. D., Wise, R. A., & Bonci, A. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.040 · Cited by 716 · see citing works
McDonald, A. J., Mascagni, F., & Guo, L. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00417-3 · Cited by 689 · see citing works
Nonuniform probability of glutamate release at a hippocampal synapse.
Rosenmund, C., Clements, J., & Westbrook, G. (1993) · Science · doi:10.1126/science.7901909 · Cited by 616 · see citing works
The functional neuroanatomy of PTSD: a critical review
Liberzon, I., & Sripada, C. S. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67011-3 · Cited by 594 · see citing works
Activity in Prelimbic Cortex Is Necessary for the Expression of Learned, But Not Innate, Fears
Corcoran, K., & Quirk, G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5327-06.2007 · Cited by 580 · see citing works
CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala
Zhou, Y., Won, J., Karlsson, M. G., Zhou, M., Rogerson, T., Balaji, J., Neve, R. L., Poirazi, P., & Silva, A. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2405 · Cited by 577 · see citing works
Burgos-Robles, A., Vidal-Gonzalez, I., & Quirk, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-09.2009 · Cited by 530 · see citing works
Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression
Courtin, J., Chaudun, F., Rozeske, R. R., Karalis, N., Gonzalez-Campo, C., Wurtz, H., Abdi, A., Baufreton, J., Bienvenu, T. C. M., & Herry, C. (2014) · Nature · doi:10.1038/nature12755 · Cited by 524 · see citing works
Long-range connectivity defines behavioral specificity of amygdala neurons
Senn, V., Wolff, S. B. E., Herry, C., Grenier, F., Ehrlich, I., Gründemann, J., Fadok, J. P., Müller, C., Letzkus, J. J., & Lüthi, A. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.006 · Cited by 522 · cited 1× · see citing works
“In addition, due to reciprocity of mPFC-BLA connectivity (Little and Carter, 2013; Senn et al., 2014), experiments should also examine whether BLA synapses onto mPFC neurons exhibit fear-related plasticity.”
Contributions of Quisqualate and NMDA Receptors to the Induction and Expression of LTP
Müller, D., Joly, M., & LYNCH, G. S. (1988) · Science · doi:10.1126/science.2904701 · Cited by 513 · see citing works
A persistent postsynaptic modification mediates long-term potentiation in the hippocampus
Kauer, J. A., Malenka, R. C., & Nicoll, R. A. (1988) · Neuron · doi:10.1016/0896-6273(88)90148-1 · Cited by 497 · see citing works
Calcium-Permeable AMPA Receptor Dynamics Mediate Fear Memory Erasure
Clem, R. L., & Huganir, R. L. (2010) · Science · doi:10.1126/science.1195298 · Cited by 496 · see citing works
Self-citationA Role for the Human Dorsal Anterior Cingulate Cortex in Fear Expression
Milad, M. R., Quirk, G. J., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.032 · Cited by 485 · see citing works
Cruikshank, S. J., Urabe, H., Nurmikko, A. V., & Connors, B. W. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.025 · Cited by 459 · see citing works
Goosens, K. A., & Maren, S. (2001) · Learning & Memory · doi:10.1101/lm.37601 · Cited by 451 · see citing works
Prefrontal Control of the Amygdala
Likhtik, E., Pelletier, J. G., Paz, R., & Paré, D. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2314-05.2005 · Cited by 361 · see citing works
Synaptic Encoding of Fear Extinction in mPFC-amygdala Circuits
Cho, J.-H., Deisseroth, K., & Bolshakov, V. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.025 · Cited by 337 · see citing works
Rosenkranz, J. A., & Grace, A. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-04090.2001 · Cited by 334 · see citing works
Tsvetkov, E., Carlezon, W. A., Benes, F. M., Kandel, E. R., & Bolshakov, V. Y. (2002) · Neuron · doi:10.1016/s0896-6273(02)00645-1 · Cited by 321 · see citing works
The amygdala and medial prefrontal cortex: partners in the fear circuit
Marek, R., Strobel, C., Bredy, T. W., & Sah, P. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.248575 · Cited by 304 · see citing works
Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement
Schiller, D., Kanen, J. W., LeDoux, J. E., Monfils, M., & Phelps, E. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320322110 · Cited by 299 · see citing works
Pathway-Specific Trafficking of Native AMPARs by In Vivo Experience
Clem, R. L., & Barth, A. L. (2006) · Neuron · doi:10.1016/j.neuron.2006.01.019 · Cited by 217 · see citing works
Self-citationRapid strengthening of thalamo-amygdala synapses mediates cue–reward learning
Tye, K. M., Stuber, G. D., de Ridder, B., Bonci, A., & Janak, P. H. (2008) · Nature · doi:10.1038/nature06963 · Cited by 216 · see citing works
Little, J. P., & Carter, A. G. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2385-13.2013 · Cited by 173 · see citing works
Consolidation of CS and US representations in associative fear conditioning
Frankland, P., Josselyn, S., Anagnostaras, S., Kogan, J., Takahashi, E., & Silva, A. J. (2004) · Hippocampus · doi:10.1002/hipo.10208 · Cited by 158 · see citing works
AMPA receptor exchange underlies transient memory destabilization on retrieval
Hong, I., Kim, J., Kim, J., Lee, S., Ko, H.-G., Nader, K., Kaang, B.-K., Tsien, R. W., & Choi, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305235110 · Cited by 148 · see citing works
Hübner, C., Bosch, D., Gall, A., Lüthi, A., & Ehrlich, I. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00064 · Cited by 115 · see citing works
Morozov, A., Sukato, D. C., & Ito, W. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5537-10.2011 · Cited by 44 · see citing works
Lin, H., Tseng, Y.-C., Mao, S.-C., Chen, P.-S., & Gean, P. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0979-11.2011 · Cited by 42 · see citing works
Fear signaling in the prelimbic-amygdala circuit: a computational modeling and recording study
Pendyam, S., Bravo-Rivera, C., Burgos-Robles, A., Sotres-Bayón, F., Quirk, G. J., & Nair, S. S. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00961.2012 · Cited by 35 · see citing works
Norepinephrine Enhances a Discrete Form of Long-Term Depression during Fear Memory Storage
Clem, R. L., & Huganir, R. L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3317-12.2013 · Cited by 33 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Resolving the neural circuits of anxiety
Calhoon, G. G., & Tye, K. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4101 · Cited by 766 · see citing works
The Role of the Medial Prefrontal Cortex in the Conditioning and Extinction of Fear
Giustino, T. F., & Maren, S. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00298 · Cited by 519 · see citing works
Fear extinction requires infralimbic cortex projections to the basolateral amygdala
Bloodgood, D. W., Sugam, J. A., Holmes, A., & Kash, T. L. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0106-x · Cited by 229 · see citing works
Prefrontal somatostatin interneurons encode fear memory
Cummings, K. A., & Clem, R. L. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0552-7 · Cited by 209 · see citing works
Self-citationThe mouse prefrontal cortex: Unity in diversity
Le Merre, P., Ährlund-Richter, S., & Carlén, M. (2021) · Neuron · doi:10.1016/j.neuron.2021.03.035 · Cited by 207 · see citing works
Sex- and Estrus-Dependent Differences in Rat Basolateral Amygdala
Blume, S. R., Freedberg, M., Vantrease, J., Chan, R., Padival, M., Record, M. J., DeJoseph, M. R., Urban, J. H., & Rosenkranz, J. A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0758-17.2017 · Cited by 182 · see citing works
Manipulating fear associations via optogenetic modulation of amygdala inputs to prefrontal cortex
Klavir, O., Prigge, M., Sarel, A., Paz, R., & Yizhar, O. (2017) · Nature Neuroscience · doi:10.1038/nn.4523 · Cited by 163 · see citing works
Optogenetic Examination of Prefrontal-Amygdala Synaptic Development
Arruda-Carvalho, M., Wu, W., Cummings, K. A., & Clem, R. L. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3097-16.2017 · Cited by 142 · see citing works
Self-citationOrexin signaling in GABAergic lateral habenula neurons modulates aggressive behavior in male mice
Flanigan, M. E., Aleyasin, H., Li, L., Burnett, C. J., Chan, K. L., LeClair, K. B., Lucas, E. K., Matikainen‐Ankney, B. A., Cuttoli, R. D.-D., Takahashi, A., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0617-7 · Cited by 147 · see citing works
Self-citationPrefrontal Cortex Drives Distinct Projection Neurons in the Basolateral Amygdala
McGarry, L. M., & Carter, A. G. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.046 · Cited by 141 · see citing works
Tan, T., Wang, W., Liu, T., Zhong, P., Conrow‐Graham, M., Tian, X., & Yan, Z. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108874 · Cited by 103 · see citing works
Multimodal and Site-Specific Plasticity of Amygdala Parvalbumin Interneurons after Fear Learning
Lucas, E. K., Jegarl, A. M., Morishita, H., & Clem, R. L. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.032 · Cited by 96 · see citing works
Self-citationThe neurocircuitry of remote cued fear memory
Bergstrom, H. C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.028 · Cited by 92 · see citing works
Guadagno, A., Belliveau, C., Mechawar, N., & Walker, C. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.669120 · Cited by 92 · see citing works
Honeycutt, J. A., Demaestri, C., Peterzell, S., Silveri, M. M., Cai, X., Kulkarni, P. P., Cunningham, M. G., Ferris, C. F., & Brenhouse, H. C. (2020) · eLife · doi:10.7554/elife.52651 · Cited by 93 · see citing works
New learning and unlearning: strangers or accomplices in threat memory attenuation?
Clem, R. L., & Schiller, D. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.03.003 · Cited by 90 · see citing works
Self-citationSex Differences in the Development of the Rodent Corticolimbic System
Premachandran, H., Zhao, M., & Arruda-Carvalho, M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.583477 · Cited by 89 · see citing works
Self-citationPrefrontal-amygdala fear networks come into focus
Arruda-Carvalho, M., & Clem, R. L. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00145 · Cited by 84 · see citing works
Self-citationMechanisms 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
GABAergic interneurons: The orchestra or the conductor in fear learning and memory?
Lucas, E. K., & Clem, R. L. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.11.016 · Cited by 77 · see citing works
Self-citationHowland, J. G., Ito, R., Lapish, C. C., & Villaruel, F. R. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104569 · Cited by 77 · see citing works
WHEN SCIENTIFIC PARADIGMS LEAD TO TUNNEL VISION: LESSONS FROM THE STUDY OF FEAR
Paré, D., & Quirk, G. (2017) · npj Science of Learning · doi:10.1038/s41539-017-0007-4 · Cited by 71 · see citing works
Jurik, A., Auffenberg, E., Klein, S., Deussing, J. M., Schmid, R. M., Wotjak, C. T., & Thoeringer, C. K. (2015) · Pain · doi:10.1097/j.pain.0000000000000318 · Cited by 72 · see citing works
Wang, Z., Shwani, T., Liu, J., Zhong, P., Yang, F., Schatz, K. C., Zhang, F., Pralle, A., & Yan, Z. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01574-y · Cited by 66 · see citing works
Prefrontal circuit organization for executive control
Kamigaki, T. (2018) · Neuroscience Research · doi:10.1016/j.neures.2018.08.017 · Cited by 65 · see citing works
Neurobiological Approach of Catatonia and Treatment Perspectives
Ellul, P., & Choucha, W. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00182 · Cited by 57 · see citing works
Gongwer, M. W., Klune, C. B., Couto, J., Jin, B., Enos, A. S., Chen, R., Friedmann, D., & DeNardo, L. A. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0697-23.2023 · Cited by 51 · see citing works
Prelimbic cortex drives discrimination of non-aversion via amygdala somatostatin interneurons
Stujenske, J. M., O’Neill, P.-K., Fernandes-Henriques, C., Nahmoud, I., Goldburg, S. R., Singh, A., Diaz, L., Labkovich, M., Hardin, W., Bolkan, S. S., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.03.020 · Cited by 50 · see citing works
Kuniishi, H., Yamada, D., Wada, K., Yamada, M., & Sekiguchi, M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0837-3 · Cited by 47 · see citing works
Organizational principles of amygdalar input-output neuronal circuits
Huang, L., Chen, Y., Jin, S., Lin, L., Duan, S., Si, K., Gong, W., & Zhu, J. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01262-3 · Cited by 44 · see citing works
McCullough, K. M., Morrison, F. G., & Ressler, K. J. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.025 · Cited by 45 · see citing works
Pathway-specific alterations of cortico-amygdala transmission in an arthritis pain model
Kiritoshi, T., & Neugebauer, V. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00022 · Cited by 44 · see citing works
Limited prefrontal cortical regulation over the basolateral amygdala in adolescent rats
Selleck, R. A., Zhang, W., Mercier, H. D., Padival, M., & Rosenkranz, J. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-35649-0 · Cited by 45 · see citing works
McGinnis, M. M., Parrish, B. C., Chappell, A. M., Alexander, N. J., & McCool, B. A. (2019) · eNeuro · doi:10.1523/eneuro.0132-19.2019 · Cited by 44 · see citing works
Reciprocal amygdala–prefrontal interactions in learning
Yizhar, O., & Klavir, O. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.06.006 · Cited by 44 · see citing works
Vila-Verde, C., Marinho, A. L. Z., Lisboa, S. F. D. S., & Guimarães, F. S. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.040 · Cited by 43 · see citing works
Song, C., & Moyer, J. R. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00146.2017 · Cited by 40 · see citing works
Mixed selectivity encoding and action selection in the prefrontal cortex during threat assessment
Grunfeld, I. S., & Likhtik, E. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.01.008 · Cited by 38 · see citing works
Bukalo, O., Nonaka, M., Weinholtz, C., Mendez, A., Taylor, W. W., & Holmes, A. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112913 · Cited by 30 · see citing works
Ariza-Salamanca, D. F., Corrales-Hernández, M. G., Pachón-Londoño, M. J., & Hernández-Duarte, I. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.993671 · Cited by 37 · see citing works
Ferrara, N. C., Trask, S., & Rosenkranz, J. (2021) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.021 · Cited by 26 · see citing works
Guthman, E. M., Garcia, J. D., Ma, M., Chu, P., Baca, S. M., Smith, K. R., Restrepo, D., & Huntsman, M. M. (2020) · eLife · doi:10.7554/elife.50601 · Cited by 32 · see citing works
Learning-induced intrinsic and synaptic plasticity in the rodent medial prefrontal cortex
Porter, J. T., & Sepulveda-Orengo, M. T. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107117 · Cited by 30 · see citing works
Kuniishi, H., Nakatake, Y., Sekiguchi, M., & Yamada, M. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01358-6 · Cited by 30 · see citing works
Price, M. E., & McCool, B. A. (2021) · Alcohol · doi:10.1016/j.alcohol.2021.08.001 · Cited by 28 · see citing works
Medial prefrontal cortex neuropeptide Y modulates binge-like ethanol consumption in C57BL/6J mice
Robinson, S. L., Marrero, I. M., Perez-Heydrich, C. A., Sepulveda-Orengo, M. T., Reissner, K. J., & Thiele, T. E. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-018-0310-7 · Cited by 28 · see citing works
Dorsal peduncular cortex activity modulates affective behavior and fear extinction in mice
Botterill, J., Khlaifia, A., Appings, R., Wilkin, J., Violi, F., Premachandran, H., Cruz-Sanchez, A., Canella, A. E., Patel, A. V., Zaidi, S., et al. (2023) · bioRxiv · doi:10.1038/s41386-024-01795-5 · Cited by 25 · see citing works
Self-citationObray, J. D., Landin, J. D., Vaughan, D. T., Scofield, M. D., & Chandler, L. J. (2022) · Addiction Neuroscience · doi:10.1016/j.addicn.2022.100044 · Cited by 26 · see citing works
Might the olfactory bulb be an origin of olfactory auras in focal epilepsy?
Sarnat, H. B., & Flores‐Sarnat, L. (2016) · Epileptic Disorders · doi:10.1684/epd.2016.0869 · Cited by 26 · see citing works
Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory
Quiñones-Laracuente, K., Vega-Medina, A., & Quirk, G. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.665116 · Cited by 25 · see citing works
Grossman, Y. S., Fillinger, C., Manganaro, A., Voren, G., Waldman, R. N., Zou, T., Janssen, W. G. M., Kenny, P. J., & Dumitriu, D. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01229-6 · Cited by 24 · see citing works
An epigenetic mechanism for over-consolidation of fear memories
Barchiesi, R., Chanthongdee, K., Petrella, M., Li, X., Söderholm, S., Domi, E., Augier, G., Coppola, A., Wiskerke, J., Szczot, I., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01758-6 · Cited by 23 · see citing works
Functional neuroimaging in patients with catatonia: A systematic review
Duque, L., Ghafouri, M., Núñez, N. A., Ospina, J. P., Philbrick, K. L., Port, J. D., Savica, R., Prokop, L. J., Rummans, T. A., & Singh, B. (2024) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2024.111640 · Cited by 21 · see citing works
Differential Alterations in Cortico-Amygdala Circuitry in Mice with Impaired Fear Extinction
Park, K., & Chung, C. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-01741-3 · Cited by 21 · see citing works
Stress can affect mitochondrial energy metabolism and AMPK/SIRT1 signaling pathway in rats
Zhao, A.-R., Li, J., Wang, S., Bian, L.-H., Li, W., & Guo, J. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.110770 · Cited by 19 · see citing works
Tryon, S. C., Bratsch-Prince, J. X., Warren, J., Jones, G. C., McDonald, A. J., & Mott, D. D. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2545-21.2022 · Cited by 18 · see citing works
Gioia, D. A., Alexander, N. J., & McCool, B. A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1785-16.2016 · Cited by 18 · see citing works
Gasnier, M., Pélissolo, A., Bondolfi, G., Pelissolo, S., Tomba, M., Mallet, L., & N’Diaye, K. (2016) · L Encéphale · doi:10.1016/j.encep.2016.10.004 · Cited by 19 · see citing works
Developmentally distinct architectures in top–down pathways controlling threat avoidance
Klune, C. B., Goodpaster, C. M., Gongwer, M. W., Gabriel, C., An, J., Chen, R., Jones, N. S., Williams, O. H., Shari, M., Ramirez, M., et al. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01890-w · Cited by 26 · see citing works
Kirry, A. J., Twining, R. C., & Gilmartin, M. R. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107249 · Cited by 16 · see citing works
Ghoweri, A. O., Gagolewicz, P. J., Frazier, H. N., Gant, J. C., Andrew, R. D., Bennett, B. M., & Thibault, O. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200617 · Cited by 16 · see citing works
Namkung, H., Thomas, K. L., Hall, J., & Sawa, A. (2021) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.12.025 · Cited by 12 · see citing works
Haikonen, J., Englund, J., Amarilla, S. P., Kharybina, Z., Shintyapina, A. B., Kegler, K., Garcia, M. S., Atanasova, T., Taira, T., Hartung, H., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105724 · Cited by 15 · see citing works
Tudi, A., Yao, M., Tang, F., Zhou, J., Li, A., Gong, H., Jiang, T., & Li, X. (2024) · BMC Biology · doi:10.1186/s12915-024-01880-7 · Cited by 15 · see citing works
Mattera, A., Pagani, M., & Baldassarre, G. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.569108 · Cited by 15 · see citing works
Díaz, F. C., Kramar, C. P., Hernandez, M. A., & Medina, J. H. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00209 · Cited by 14 · see citing works
Zeisler, Z. R., Heslin, K. A., Stoll, F. M., Hof, P. R., Clem, R. L., & Rudebeck, P. H. (2024) · Current Biology · doi:10.1016/j.cub.2024.06.012 · Cited by 13 · see citing works
Self-citationCrofton, E. J., Zhu, M., Curtis, K. N., Nolan, G. W., O’Buckley, T. K., Morrow, A. L., & Herman, M. A. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108912 · 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
Oxytocin modulation in the medial prefrontal cortex of pair-exposed rats during fear conditioning
Jang, M., Jung, T., Jeong, Y., Byun, Y., & Noh, J. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105752 · Cited by 12 · see citing works
The Role of Basolateral Amygdala and Medial Prefrontal Cortex in Fear: A Systematic Review
Mavrych, V., Riyas, F., & Bolgova, O. (2025) · Cureus · doi:10.7759/cureus.78198 · Cited by 12 · see citing works
Developmental emergence of persistent memory for contextual and auditory fear in micePreprint
Samifanni, R., Zhao, M., Cruz-Sanchez, A., Satheesh, A., Mumtaz, U., & Arruda-Carvalho, M. (2021) · Learning & Memory · doi:10.1101/lm.053471.121 · Cited by 13 · see citing works
Self-citationRobakiewicz, I., Polak, M., Rawska, M., Alberski, D., Polowy, R., Wytrychiewicz, K., Syperek, M., Matysiak, J., & Filipkowski, R. (2019) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2019-029 · Cited by 10 · see citing works
TREK-1 inhibition promotes synaptic plasticity in the prelimbic cortex
de Oliveira, J. F., Higa, G. S. V., Viana, F. J. C., Cruvinel, E., Carlos-Lima, E., Borges, F. S., Zampieri, T. T., Rebello, F. P., Ulrich, H., & Pasquale, R. D. (2023) · Experimental Neurology · doi:10.1016/j.expneurol.2023.114652 · Cited by 10 · see citing works
PV-dependent reorganization of prelimbic cortex sub-engrams during systems consolidation
Golbabaei, A., Josselyn, S. A., & Frankland, P. W. (2025) · Neuron · doi:10.1016/j.neuron.2025.09.033 · Cited by 9 · see citing works
Cyfip1 Regulates SynGAP1 at Hippocampal Synapses
Sahasrabudhe, A., Begum, F., Guevara, C. A., Morrison, C., Hsiao, K., Kezunovic, N., Bozdagi-Gunal, O., & Benson, D. L. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.581714 · Cited by 8 · see citing works
Tavares, G. E. B., Bianchi, P., Yokoyama, T. S., Palombo, P., & Cruz, F. C. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114435 · Cited by 8 · see citing works
Ex Vivo Optogenetic Dissection of Fear Circuits in Brain Slices
Bosch, D., Asede, D., & Ehrlich, I. (2016) · Journal of Visualized Experiments · doi:10.3791/53628 · Cited by 7 · see citing works
Ethanol modulation of cortico-basolateral amygdala circuits: Neurophysiology and behavior
McCool, B. A. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108750 · Cited by 7 · see citing works
Cruz-Sanchez, A., LaDouceur, K. E., Abdusalom, A., Chasiotis, H., Gugustea, R., Inayat, M., Mumtaz, U., Hasantash, M., Anacker, C., & Arruda-Carvalho, M. (2026) · Cell Reports · doi:10.1016/j.celrep.2025.116812 · Cited by 9 · see citing works
Self-citationLi, X., Hao, S., Zou, S., Tu, X., Kong, W., Jiang, T., & Chen, J.-G. (2023) · Molecular Autism · doi:10.1186/s13229-023-00567-0 · Cited by 7 · see citing works
Excitation of prefrontal cortical neurons during conditioning enhances fear memory formation
Shibano, N., Yamazaki, M., Arima, T., Abe, K., Kuroda, M., Kobayashi, Y., Itohara, S., Furuichi, T., & Sano, Y. (2020) · Scientific Reports · doi:10.1038/s41598-020-65597-7 · Cited by 5 · see citing works
Klenowski, P. M., Fogarty, M., Drieberg-Thompson, J. R., Bellingham, M., & Bartlett, S. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.10.039 · Cited by 8 · see citing works
Developmentally distinct architectures in top-down circuitsPreprint
Klune, C. B., Goodpaster, C. M., Gongwer, M. W., Gabriel, C., Chen, R., Jones, N. S., Schwarz, L. A., & DeNardo, L. A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.27.555010 · Cited by 7 · see citing works
Sánchez-Hidalgo, A. C., Arias-Aragón, F., Romero-Barragán, M. T., Martín-Cuevas, C., Delgado-Garcia, J. M., Martı́nez-Mir, A., & Scholl, F. G. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113896 · Cited by 6 · see citing works
Bertocchi, I., Rocha-Almeida, F., Romero-Barragán, M. T., Cambiaghi, M., Carretero‐Guillén, A., Botta, P., Dogbevia, G., Treviño, M., Mele, P., Oberto, A., et al. (2023) · iScience · doi:10.1016/j.isci.2023.108050 · Cited by 6 · see citing works
Santos, T. B., Soares, J. C. K., Coelho, C. A. O., & Oliveira, M. G. M. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad375 · Cited by 8 · see citing works
Shin, D., Cho, E., Park, K., Chung, C., Kim, D. H., Jeon, S. J., & Shin, C. Y. (2025) · Animal Cells and Systems · doi:10.1080/19768354.2025.2493258 · Cited by 5 · see citing works
Medial prefrontal cortex circuit dynamics involved in stage-specific addiction
Dongdong, Z., Zhang, X., & Bai, J. (2025) · Brain Structure and Function · doi:10.1007/s00429-025-03055-8 · Cited by 5 · see citing works
Neuronal tuning to threat exposure remains stable in the mouse prefrontal cortex over multiple days
Sylte, O. C., Muysers, H., Chen, H.-L., Bartos, M., & Sauer, J. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002475 · Cited by 5 · see citing works
Xie, H., Wu, D., Gao, X., Wang, N., & Xiao, Z. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.05.038 · Cited by 5 · see citing works
Responsivity of lateral septum-mPFC connections in alloxan-induced hyperglycemia
Contreras, C. M., Gutiérrez‐García, A. G., & Moreno-Cortés, M. L. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.111919 · Cited by 5 · see citing works
Orexin signaling in GABAergic lateral habenula neurons modulates aggressive behaviorPreprint
Flanigan, M. E., Aleyasin, H., Li, L., Burnett, C. J., Chan, K. L., LeClair, K. B., Lucas, E. K., Matikainen‐Ankney, B. A., Janssen, W. F., Takahashi, A., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/811265 · Cited by 4 · see citing works
Self-citationVazquez, K., & Parsons, R. G. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.07.611834 · Cited by 4 · see citing works
Lozano, K., Felix‐Ortiz, A. C., Terrell, J. M., Gonzalez, C., Whitehorn, K. R., Kanke, A. E., Villalon, S. A., Ramos, A. R., Miller, A. N., Rodríguez-Romaguera, J., et al. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02073-8 · Cited by 3 · see citing works
Arias-Aragón, F., Sánchez-Hidalgo, A. C., Gruart, A., Martı́nez-Mir, A., Delgado-Garcia, J. M., & Scholl, F. G. (2025) · Experimental Neurology · doi:10.1016/j.expneurol.2025.115241 · Cited by 3 · see citing works
Fernandes-Henriques, C., Guetta, Y., Sclar, M., Zhang, R., Miura, Y., Surrence, K., Friedman, A. K., & Likhtik, E. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1001-24.2025 · Cited by 3 · see citing works
Tu, Z., Ma, Y., Shang, H., Zhao, S., Xue, B., Qu, Y., Chen, J., Li, Y., Hu, J., Gao, F., et al. (2024) · Neuropsychopharmacology · doi:10.1038/s41386-024-02029-4 · Cited by 3 · see citing works
Premachandran, H., Wilkin, J., & Arruda-Carvalho, M. (2024) · Current Protocols · doi:10.1002/cpz1.1040 · Cited by 2 · see citing works
Self-citationMorishima, M., Matsumura, S., Tohyama, S., Nagashima, T., Konno, A., Hirai, H., & Watabe, A. M. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1292822 · Cited by 2 · see citing works
- Authors
- Arruda-Carvalho, M., & Clem, R. L.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-11-19
- Volume
- 34
- Issue
- 47
- Pages
- 15601-15609
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6608438
- OpenAlex
- W2039010512
- Cited by
- 127
- References
- 44
- Citations by year
- 2026: 9 · 2025: 11 · 2024: 11 · 2023: 11 · 2022: 12 · 2021: 17 · 2020: 14 · 2019: 8 · 2018: 9 · 2017: 9 · 2016: 10 · 2015: 6
- FWCI
- 4.65
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (R01MH105414)
- 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
- fear conditioning, basolateral amygdala, medial prefrontal cortex, infralimbic cortex, prelimbic cortex, synaptic plasticity, feedforward inhibition, excitation-inhibition balance
- MeSH terms
- Amygdala, Animals, Fear, Male, Mice, Inbred C57BL, Neural Pathways, Synaptic Transmission, Neuronal Plasticity, Prefrontal Cortex, Receptors, AMPA, Excitatory Postsynaptic Potentials, Mice, Electrophysiological Phenomena
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