A thalamic-hippocampal CA1 signal for contextual fear memory suppression, extinction, and discrimination
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Abstract
The adaptive regulation of fear memories is a crucial neural function that prevents inappropriate fear expression. Fear memories can be acquired through contextual fear conditioning (CFC) which relies on the hippocampus. The thalamic nucleus reuniens (NR) is necessary to extinguish contextual fear and innervates hippocampal CA1. However, the role of the NR-CA1 pathway in contextual fear is unknown. We developed a head-restrained virtual reality CFC paradigm, and demonstrate that mice can acquire and extinguish context-dependent fear responses. We found that inhibiting the NR-CA1 pathway following CFC lengthens the duration of fearful freezing epochs, increases fear generalization, and delays fear extinction. Using in vivo imaging, we recorded NR-axons innervating CA1 and found that NR-axons become tuned to fearful freezing following CFC. We conclude that the NR-CA1 pathway actively suppresses fear by disrupting contextual fear memory retrieval in CA1 during fearful freezing behavior, a process that also reduces fear generalization and accelerates extinction.
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These ROIs have been previously associated with fear memory and align with work at the circuit level.
“These ROIs have been previously associated with fear memory56,59-66 and align with work at the circuit level62.”
From Magnetic resonance microscopy maps widespread effects of Alzheimer’s disease on brain structures and behavior in mice (2026) · cites this paper as [62]
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Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
XGBoost: A Scalable Tree Boosting System
Chen, T., & Guestrin, C. (2016) · Proceedings of the 22nd ACM SIGKDD International Conference on Knowledge Discovery and Data Mining · doi:10.1145/2939672.2939785 · Cited by 54,569 · see citing works
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
U1 snRNP regulates cancer cell migration and invasion in vitro
Oh, J.-M., Venters, C. C., Di, C., Pinto, A. M., Wan, L., Younis, I., Cai, Z., Arai, C., So, B. R., Duan, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-13993-7 · Cited by 7,157 · see citing works
Anomalous collapses of Nares Strait ice arches leads to enhanced export of Arctic sea ice
Moore, G. W. K., Howell, S. E. L., Brady, M., Xu, X., & McNeil, K. (2021) · Nature Communications · doi:10.1038/s41467-020-20314-w · Cited by 5,155 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Neurobiology of Pavlovian Fear Conditioning
Maren, S. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.897 · Cited by 1,805 · see citing works
Roth, B. L. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.040 · Cited by 1,742 · see citing works
Optogenetic stimulation of a hippocampal engram activates fear memory recall
Liu, X., Ramirez, S., Pang, P. T., Puryear, C. B., Govindarajan, A., Deisseroth, K. A., & Tonegawa, S. (2012) · Nature · doi:10.1038/nature11028 · Cited by 1,669 · see citing works
Rapid, reversible activation of AgRP neurons drives feeding behavior in mice
Krashes, M. J., Koda, S., Ye, C., Rogan, S. C., Adams, A. C., Cusher, D. S., Maratos-Flier, E., Roth, B. L., & Lowell, B. B. (2011) · Journal of Clinical Investigation · doi:10.1172/jci46229 · Cited by 1,578 · 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
Suite2p: beyond 10,000 neurons with standard two-photon microscopyPreprint
Pachitariu, M., Stringer, C., Dipoppa, M., Schröder, S., Rossi, L. F., Dalgleish, H. W. P., Carandini, M., & Harris, K. D. (2016) · bioRxiv · doi:10.1101/061507 · Cited by 1,150 · see citing works
Memory Reconsolidation and Extinction Have Distinct Temporal and Biochemical Signatures
Suzuki, A., Josselyn, S. A., Frankland, P. W., Masushige, S., Silva, A. J., & Kida, S. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5491-03.2004 · Cited by 1,127 · see citing works
Crouching as an index of fear.
Blanchard, R. J., & Blanchard, D. C. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0026779 · Cited by 1,077 · see citing works
Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles
Guzowski, J. F., McNaughton, B. L., Barnes, C. A., & Worley, P. F. (1999) · Nature Neuroscience · doi:10.1038/16046 · Cited by 1,032 · see citing works
Wood, E. R., Dudchenko, P. A., Robitsek, R. J., & Eichenbaum, H. (2000) · Neuron · doi:10.1016/s0896-6273(00)00071-4 · Cited by 992 · see citing works
Functional imaging of hippocampal place cells at cellular resolution during virtual navigation
Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L., & Tank, D. W. (2010) · Nature Neuroscience · doi:10.1038/nn.2648 · Cited by 873 · see citing works
Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat
Steward, O., & Scoville, S. A. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901690306 · Cited by 837 · see citing works
Vertes, R. P. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.06.027 · Cited by 811 · see citing works
Mapping of a non-spatial dimension by the hippocampal-entorhinal circuit
Aronov, D., Nevers, R., & Tank, D. W. (2017) · Nature · doi:10.1038/nature21692 · Cited by 773 · see citing works
A Neural Circuit for Memory Specificity and Generalization
Xu, W., & Südhof, T. C. (2013) · Science · doi:10.1126/science.1229534 · Cited by 634 · 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
Dynamics of Retrieval Strategies for Remote Memories
Goshen, I., Brodsky, M., Prakash, R., Wallace, J. L., Gradinaru, V., Ramakrishnan, C., & Deisseroth, K. A. (2011) · Cell · doi:10.1016/j.cell.2011.09.033 · Cited by 546 · 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
Dendritic Inhibition in the Hippocampus Supports Fear Learning
Lovett-Barron, M., Kaifosh, P., Kheirbek, M. A., Danielson, N., Zaremba, J. D., Reardon, T. R., Turi, G. F., Hen, R., Zemelman, B. V., & Losonczy, A. (2014) · Science · doi:10.1126/science.1247485 · Cited by 509 · see citing works
Projections from neocortex mediate top-down control of memory retrieval
Rajasethupathy, P., Sankaran, S., Marshel, J. H., Kim, C. K., Ferenczi, E., Lee, S. Y., Berndt, A., Ramakrishnan, C., Jaffe, A., Lo, M., et al. (2015) · Nature · doi:10.1038/nature15389 · Cited by 509 · see citing works
The dorsal hippocampus is essential for context discrimination but not for contextual conditioning.
Frankland, P. W., Cestari, V., Filipkowski, R. K., McDonald, R. J., & Silva, A. J. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.4.863 · Cited by 486 · see citing works
Herkenham, M. A. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901770405 · Cited by 479 · see citing works
Generalized Anxiety Disorder Is Associated With Overgeneralization of Classically Conditioned Fear
Lissek, S. M., Kaczkurkin, A. N., Rabin, S. J., Geraci, M. F., Pine, D. S., & Grillon, C. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.025 · Cited by 462 · see citing works
Nagai, Y., Miyakawa, N., Takuwa, H., Hori, Y., Oyama, K., Ji, B., Takahashi, M., Huang, X., Slocum, S. T., DiBerto, J. F., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0661-3 · Cited by 408 · see citing works
Limbic circuitry of the midline thalamus
Vertes, R. P., Linley, S. B., & Hoover, W. B. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.014 · Cited by 391 · see citing works
Parallel emergence of stable and dynamic memory engrams in the hippocampus
Hainmueller, T., & Bartos, M. (2018) · Nature · doi:10.1038/s41586-018-0191-2 · Cited by 383 · see citing works
Garfinkel, S. N., Abelson, J. L., King, A. P. J., Sripada, R. K., Wang, X., Gaines, L. M., & Liberzon, I. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4287-13.2014 · Cited by 361 · see citing works
Wouterlood, F. G., Saldana, E., & Witter, M. P. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902960202 · Cited by 328 · see citing works
Distinct hippocampal engrams control extinction and relapse of fear memory
Lacagnina, A. F., Brockway, E. T., Crovetti, C. R., Shue, F., McCarty, M. J., Sattler, K. P., Lim, S. C., Santos, S. L., Denny, C. A., & Drew, M. R. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0361-z · Cited by 311 · see citing works
Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat
Vertes, R. P., Hoover, W. B., Valle, A. C., Sherman, A., & Rodriguez, J. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21135 · Cited by 305 · see citing works
Chemogenetic Interrogation of a Brain-wide Fear Memory Network in Mice
Vetere, G., Kenney, J. W., Tran, L. M., Xia, F., Steadman, P. E., Parkinson, J., Josselyn, S. A., & Frankland, P. W. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.037 · Cited by 293 · see citing works
Encoding of contextual fear memory in hippocampal–amygdala circuit
Kim, W. B., & Cho, J.-H. (2020) · Nature Communications · doi:10.1038/s41467-020-15121-2 · Cited by 289 · see citing works
Afferent projections to nucleus reuniens of the thalamus
McKenna, J. T., & Vertes, R. P. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20342 · Cited by 272 · see citing works
Vertes, R. P. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.10083 · Cited by 266 · see citing works
In vivo measurement of afferent activity with axon-specific calcium imaging
Broussard, G. J., Liang, Y., Fridman, M. V., Unger, E. K., Meng, G., Xiao, X., Ji, N., Petreanu, L., & Tian, L. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0211-4 · Cited by 222 · see citing works
Sun, Y., Nguyen, A. Q., Nguyen, J. P., Le, L., Saur, D., Choi, J., Callaway, E. M., & Xu, X. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.02.030 · Cited by 218 · see citing works
Increased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation
Sheffield, M. E. J., Adoff, M. D., & Dombeck, D. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.029 · Cited by 214 · see citing works
Self-citationAn action potential initiation mechanism in distal axons for the control of dopamine release
Liu, C., Cai, X., Ritzau-Jost, A., Kramer, P. F., Li, Y., Khaliq, Z. M., Hallermann, S., & Kaeser, P. S. (2022) · Science · doi:10.1126/science.abn0532 · Cited by 213 · see citing works
Hippocampal awake replay in fear memory retrieval
Wu, C.-T., Haggerty, D., Kemere, C., & Ji, D. (2017) · Nature Neuroscience · doi:10.1038/nn.4507 · Cited by 210 · see citing works
Distinct place cell dynamics in CA1 and CA3 encode experience in new environments
Dong, C., Madar, A. D., & Sheffield, M. E. J. (2021) · Nature Communications · doi:10.1038/s41467-021-23260-3 · Cited by 209 · see citing works
Self-citationder Weel, M. J. D.-V., Griffin, A. L., Ito, H., Shapiro, M. L., Witter, M. P., Vertes, R. P., & Allen, T. A. (2019) · Learning & Memory · doi:10.1101/lm.048389.118 · Cited by 201 · see citing works
Ji, J.-Z., & Maren, S. (2008) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.794808 · Cited by 195 · see citing works
Kaufman, A. M., Geiller, T., & Losonczy, A. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.029 · Cited by 193 · see citing works
der Weel, M. J. D.-V., Lopes, F. H. D. S., & Witter, M. P. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05640.1997 · Cited by 189 · see citing works
Hoover, W. B., & Vertes, R. P. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0345-6 · Cited by 178 · see citing works
Gabbott, P. L. A., & Bacon, S. J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960122)364:4 · Cited by 165 · see citing works
Orchestrated ensemble activities constitute a hippocampal memory engram
Ghandour, K., Ohkawa, N., Fung, C. C. A., Asai, H., Saitoh, Y., Takekawa, T., Okubo-Suzuki, R., Soya, S., Nishizono, H., Matsuo, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10683-2 · Cited by 162 · see citing works
Zhu, H., Pleil, K. E., Urban, D. J., Moy, S. S., Kash, T. L., & Roth, B. L. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.35 · Cited by 158 · see citing works
An Integrated Index: Engrams, Place Cells, and Hippocampal Memory
Goode, T. D., Tanaka, K. Z., Sahay, A., & McHugh, T. J. (2020) · Neuron · doi:10.1016/j.neuron.2020.07.011 · Cited by 158 · see citing works
Bidirectional synaptic plasticity rapidly modifies hippocampal representations
Milstein, A. D., Li, Y., Bittner, K. C., Grienberger, C., Soltesz, I., Magee, J. C., & Romani, S. (2021) · eLife · doi:10.7554/elife.73046 · Cited by 151 · see citing works
Thalamic excitation of hippocampal CA1 neurons: a comparison with the effects of CA3 stimulation
Bertram, E. H., & Zhang, D. X. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00712-x · Cited by 143 · see citing works
Prefrontal projections to the thalamic nucleus reuniens mediate fear extinction
Ramanathan, K. R., Jin, J., Giustino, T. F., Payne, M. R., & Maren, S. (2018) · Nature Communications · doi:10.1038/s41467-018-06970-z · Cited by 140 · see citing works
All-optical physiology resolves a synaptic basis for behavioral timescale plasticity
Fan, L. Z., Kim, D. K., Jennings, J. H., Tian, H., Wang, P. Y., Ramakrishnan, C., Randles, S., Sun, Y., Thadhani, E., Kim, Y. S., et al. (2023) · Cell · doi:10.1016/j.cell.2022.12.035 · Cited by 135 · see citing works
Kim, W. B., & Cho, J.-H. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3579-16.2017 · Cited by 131 · see citing works
Slow integration leads to persistent action potential firing in distal axons of coupled interneurons
Sheffield, M. E. J., Best, T. K., Mensh, B. D., Kath, W. L., & Spruston, N. (2011) · Nature Neuroscience · doi:10.1038/nn.2728 · Cited by 125 · see citing works
Self-citationSignatures of rapid plasticity in hippocampal CA1 representations during novel experiences
Priestley, J. B., Bowler, J. C., Rolotti, S. V., Fusi, S., & Losonczy, A. (2022) · Neuron · doi:10.1016/j.neuron.2022.03.026 · Cited by 122 · see citing works
Kajiwara, R., Wouterlood, F. G., Sah, A., Boekel, A. J., Baks‐te‐Bulte, L., & Witter, M. P. (2007) · Hippocampus · doi:10.1002/hipo.20385 · Cited by 107 · see citing works
Ramanathan, K. R., Ressler, R. L., Jin, J., & Maren, S. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1429-18.2018 · Cited by 106 · see citing works
Fanselow, M. S., & Tighe, T. J. (1988) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.14.2.187 · Cited by 101 · see citing works
Krishnan, S., Heer, C. M., Cherian, C., & Sheffield, M. E. J. (2022) · Nature Communications · doi:10.1038/s41467-022-34465-5 · Cited by 97 · see citing works
Self-citationA thalamo-amygdalar circuit underlying the extinction of remote fear memories
Silva, B. A., Astori, S., Burns, A. M., Heiser, H., van den Heuvel, L., Santoni, G., Martínez-Reza, M. F., Sandi, C., & Gräff, J. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00856-y · Cited by 88 · see citing works
Activation of the infralimbic cortex in a fear context enhances extinction learningPreprint
Thompson, B. M., Baratta, M. V., Biedenkapp, J. C., Rudy, J. W., Watkins, L. R., & Maier, S. F. (2010) · Learning & Memory · doi:10.1101/lm.1920810 · Cited by 86 · see citing works
Functional heterogeneity of the limbic thalamus: From hippocampal to cortical functions
Wolff, M., Alcaraz, F., Marchand, A. R., & Coutureau, É. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.011 · Cited by 80 · see citing works
Amount of fear extinction changes its underlying mechanisms
An, B., Kim, J., Park, K., Lee, S., Song, S., & Choi, S. (2017) · eLife · doi:10.7554/elife.25224 · Cited by 76 · see citing works
Nucleus reuniens mediates the extinction of contextual fear conditioning
Ramanathan, K. R., & Maren, S. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112114 · Cited by 76 · see citing works
Troyner, F., Bicca, M. A., & Bertoglio, L. J. (2018) · Hippocampus · doi:10.1002/hipo.22964 · Cited by 73 · see citing works
Thalamic nucleus reuniens coordinates prefrontal-hippocampal synchrony to suppress extinguished fear
Totty, M. S., Tuna, T., Ramanathan, K. R., Jin, J., Peters, S. E., & Maren, S. (2023) · Nature Communications · doi:10.1038/s41467-023-42315-1 · Cited by 60 · see citing works
Chittajallu, R., Wester, J. C., Craig, M. T., Barksdale, E., Yuan, X. Q., Akgül, G., Fang, C., Collins, D., Hunt, S., Pelkey, K. A., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00218-y · Cited by 56 · see citing works
Function and mechanisms of memory destabilization and reconsolidation after retrieval
Kida, S. (2020) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.96.008 · Cited by 55 · see citing works
Nucleus reuniens transiently synchronizes memory networks at beta frequencies
Jayachandran, M., Viena, T. D., Garcia, A., Veliz, A. V., Leyva, S., Roldan, V., Vertes, R. P., & Allen, T. A. (2023) · Nature Communications · doi:10.1038/s41467-023-40044-z · Cited by 53 · see citing works
Extinction of Learned Fear Induces Hippocampal Place Cell Remapping
Wang, M. E., Yuan, R. K., Keinath, A. T., Ramos‐Álvarez, M. M., & Muzzio, I. A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4477-14.2015 · Cited by 52 · see citing works
Lee, C., Lee, B. H., Jung, H., Lee, C., Sung, Y., Kim, H., Kim, J., Shim, J. Y., Kim, J., Choi, D. I., et al. (2023) · Current Biology · doi:10.1016/j.cub.2022.12.038 · Cited by 52 · see citing works
Irreplaceability of Neuronal Ensembles after Memory Allocation
Matsuo, N. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.03.042 · Cited by 49 · see citing works
der Weel, M. J. D.-V., Lopes, F. H. D. S., & Witter, M. P. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1350-6 · Cited by 46 · see citing works
Bayer, H., & Bertoglio, L. J. (2020) · Scientific Reports · doi:10.1038/s41598-020-72856-0 · Cited by 40 · see citing works
The Quest for the Hippocampal Memory Engram: From Theories to Experimental Evidence
Miry, O., Li, J., & Chen, L. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.632019 · Cited by 32 · see citing works
Nagai, Y., Miyakawa, N., Takuwa, H., Hori, Y., Oyama, K., Ji, B., Takahashi, M., Huang, X., Slocum, S. T., DiBerto, J. F., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/854513 · Cited by 27 · see citing works
Expanding the canon: An inclusive neurobiology of thalamic and subthalamic fear circuits
Venkataraman, A., & Dias, B. G. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109380 · Cited by 26 · see citing works
Morales, G. J., Ramcharan, E. J., Sundararaman, N., Morgera, S. D., & Vertes, R. P. (2007) · Conference proceedings · doi:10.1109/iembs.2007.4352831 · Cited by 26 · see citing works
Goswamee, P., Leggett, E., & McQuiston, A. R. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.660897 · Cited by 23 · see citing works
Bidirectional synaptic plasticity rapidly modifies hippocampal representationsPreprint
Milstein, A. D., Li, Y., Bittner, K. C., Grienberger, C., Soltész, I., Magee, J. C., & Romani, S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.04.934182 · Cited by 20 · see citing works
Moscarello, J. M. (2020) · Learning & Memory · doi:10.1101/lm.050377.119 · Cited by 20 · see citing works
Andrianova, L., Banks, P. J., Booth, C. A., Brady, E. S., Margetts‐Smith, G., Kohli, S., Cavanagh, J., Bashir, Z. I., McBain, C. J., & Craig, M. T. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.30.462517 · Cited by 15 · see citing works
Sun, Q., Buss, E. W., Jiang, Y., Santoro, B., Brann, D. H., Nicholson, D. A., & Siegelbaum, S. A. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0451-20.2021 · Cited by 11 · see citing works
hmacomber/NR-Analysis: DOI archiving
R, H. (2023) · Zenodo (CERN European Organization for Nuclear Research) · doi:10.5281/zenodo.8393379 · Cited by 1 · see citing works
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Research works printed but not linked: 3
- [56]Dolleman-Van Der Weel MJ Witter MP Projections from the nucleus reuniens thalami to the entorhinal cortex, hippocampal field CA1, and the subiculum in the rat arise from different populations of neurons J. Comp. Neurol. 1996 364 637 650 8821451
- [71]Andrianova, L. et al. Hippocampal CA1 pyramidal cells do not receive monosynaptic input from thalamic nucleus reuniens. bioRxiv10.1101/2021.09.30.462517 (2021).
- [84]Heather C. et al. Code from: a thalamic-hippocampal CA1 signal for contextual fear memory suppression, extinction, and discrimination. NR Analysis at 10.5281/zenodo.8393380 (2023). PMC10598272 37875465 · DOI
Cited by
Sorted by citations
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Plas, S. L., Tuna, T., Bayer, H., Juliano, V. A. L., Sweck, S. O., Perez, A. D. A., Hassell, J. E., & Maren, S. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1352797 · Cited by 47 · see citing works
Virtual reality modulating dynamics of neuroplasticity: Innovations in neuro-motor rehabilitation
Wankhede, N. L., Koppula, S., Ballal, S., Doshi, H., Kumawat, R., Raju, S., Arora, I., Sammeta, S. S., Khalid, M., Zafar, A., et al. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.12.040 · Cited by 47 · see citing works
Brain mechanisms underlying the inhibitory control of thought
Anderson, M. C., Crespo‐García, M., & Subbulakshmi, S. (2025) · Nature reviews. Neuroscience · doi:10.1038/s41583-025-00929-y · Cited by 44 · see citing works
Kjærgaard, K., Mikkelsen, A. C. D., Landau, A. M., Eriksen, P. L., Hamilton-Dutoit, S. J., Magnusson, N. E., Thomsen, M. B., Chen, F., Vilstrup, H., Mookerjee, R. P., et al. (2023) · JHEP Reports · doi:10.1016/j.jhepr.2023.100992 · Cited by 38 · see citing works
Rao, J., Li, H., Zhang, H., Xiang, X., Ding, X., Li, L., Geng, F., & Qi, H. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.117400 · Cited by 26 · see citing works
Planetary microbiome structure and generalist-driven gene flow across disparate habitats
Kim, C. Y., Podlesny, D., Schiller, J., Khedkar, S., Fullam, A., Orakov, A. N., Schudoma, C., Robbani, S. M., Grekova, A., Kuhn, M., et al. (2026) · Cell · doi:10.1016/j.cell.2025.12.051 · Cited by 15 · see citing works
CA1 Engram Cell Dynamics Before and After LearningPreprint
Monasterio, A. H., Lienkaemper, C., Coello, S., Senne, R. A., Ocker, G. K., Scott, B. B., & Ramirez, S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.16.589790 · Cited by 15 · see citing works
Cheung, H., Yu, T.-Z., Yi, X., Wu, Y., Wang, Q., Gu, X., Xu, M., Cai, M., Wen, W., Li, X.-N., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-06417-w · Cited by 13 · see citing works
The Emerging Role of Brain Mitochondria in Fear and Anxiety
Chioino, A., & Sandi, C. (2024) · Current topics in behavioral neurosciences · doi:10.1007/7854_2024_537 · Cited by 11 · see citing works
Hippocampal ensembles regulate circuit-induced relapse of extinguished fear
Hassell, J. E., Pérez, A. D. A., Vasudevan, K., Ressler, R. L., Garcia, G. M., Parr, M., Vierkant, V., Bayer, H., & Maren, S. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03064-3 · Cited by 10 · see citing works
Panzer, É., Olmo, I. G., de Vasconcelos, A. P., Stéphan, A., & Cassel, J. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105762 · Cited by 8 · see citing works
Projections from thalamic nucleus reuniens to medial septum enable extinction of remote fear memory
Tomaszewski, K. F., Gajewska‐Woźniak, O., Ziółkowska, M., Łukasiewicz, K., Cały, A., Sotoudeh, N., Puchalska, M., Salamian, A., & Radwańska, K. (2026) · Acta Neurobiologiae Experimentalis · doi:10.55782/zd27ss41 · Cited by 7 · see citing works
Rojas, A. K. P., Linley, S. B., & Vertes, R. P. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.115066 · Cited by 5 · see citing works
Ziółkowska, M., Sotoudeh, N., Cały, A., Puchalska, M., Pagano, R., Śliwińska, M. A., Salamian, A., & Radwańska, K. (2025) · eLife · doi:10.7554/elife.101736.3 · Cited by 5 · see citing works
Amygdala‐Dependent Signaling Pathways and Regulating Circuits in Fear Memory
Huang, M.-Q., Liang, X., Lin, X., Li, W., Jiang, Y., & Geng, F. (2025) · Synapse · doi:10.1002/syn.70026 · Cited by 4 · see citing works
Luo, H., Frederick, M. H., de Velasco, E. M. F., Oltmanns, J. R. O., Wright, C. J., & Wickman, K. D. (2024) · Learning & Memory · doi:10.1101/lm.054022.124 · Cited by 4 · see citing works
Irving, Z., Greiner, E., Indriolo, M., Liu, Z., & Petrovich, G. D. (2025) · Brain Structure and Function · doi:10.1007/s00429-025-02927-3 · Cited by 2 · see citing works
Zhang, J., Zheng, X., Zhang, G., Cheng, Z., Liu, Y., Zhang, L., Zhang, J., Liu, X., & Yang, Z. (2025) · Translational Psychiatry · doi:10.1038/s41398-025-03417-0 · Cited by 6 · see citing works
Wang, H. Y., Mao, X., Liu, S., Zhang, J., Li, E., Song, Y., Li, H., Chang, L., & Wu, Y. (2025) · Journal of Alzheimer s Disease Reports · doi:10.1177/25424823251391704 · Cited by 3 · see citing works
Associative coding of conditioned fear in the thalamic nucleus reuniens in rodents and humans
Tuna, T., Totty, M. S., Badarnee, M., Mourão, F. A. G., Peters, S. E., Milad, M. R., & Maren, S. (2025) · Communications Biology · doi:10.1038/s42003-025-08580-0 · Cited by 4 · see citing works
A Preprocessing Toolbox for 2-Photon Subcellular Calcium Imaging
Jiang, A., Zhao, C., & Sheffield, M. E. J. (2025) · eNeuro · doi:10.1523/eneuro.0565-24.2025 · Cited by 3 · see citing works
Self-citationBrain Mechanisms Underlying the Inhibitory Control of ThoughtPreprint
Anderson, M. C., Crespo‐García, M., & Subbulakshmi, S. (2024) · doi:10.31234/osf.io/4wcnb · Cited by 3 · see citing works
Ziółkowska, M., Sotoudeh, N., Cały, A., Puchalska, M., Pagano, R., Śliwińska, M. A., Salamian, A., & Radwańska, K. (2024) · eLife · doi:10.7554/elife.101736.2 · Cited by 3 · see citing works
Diencephalic modulation of the hippocampus in affective and cognitive behavior
Vertes, R. P., Linley, S. B., Rojas, A. K. P., Lamothe, K., & Allen, T. A. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101377 · Cited by 2 · see citing works
SAME: Topology-flexible transforms enable robust integration of multimodal spatial omicsPreprint
Pratapa, A., Mansouri, S., Nikulina, N., Matuck, B. F., Schneider, M. A., Byrd, K. M., Savai, R., Tata, P. R., & Singh, R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.12.664419 · Cited by 2 · see citing works
Tian, Y., Hornburg, K., Austin, W., Cook, J. J., Qi, Y., White, L. E., Killmar, J. T., Kaczorowski, C. C., Ashbrook, D. G., Johnson, G. A., et al. (2026) · Nature Neuroscience · doi:10.1038/s41593-025-02199-4 · Cited by 1 · see citing works
ApoE Isoform-Dependent Effects on Extinction of Contextual Fear Memory and Passive Avoidance Memory
Saltonstall, E., Pederson, A., O’Niel, A., Holden, S. J., Kessler, K., Torres, E. R. S., & Raber, J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26125820 · Cited by 1 · see citing works
Pedroza‐Sotelo, K., Schwarb, H. D., Auerbach, R. P., Ghosh, S., Henin, A., Hofmann, S. G., Pizzagalli, D. A., Yendiki, A., Whitfield, S., Gabrieli, J. D. E., et al. (2025) · Hippocampus · doi:10.1002/hipo.70028 · Cited by 1 · see citing works
Tuna, T., Mourão, F. A. G., & Maren, S. (2025) · Brain stimulation · doi:10.1016/j.brs.2025.11.011 · Cited by 1 · see citing works
Liu, X., Wang, X., Su, H. C., Zhang, M., Bian, X., Duan, C., Wang, S., Pi, C., Nie, X., Dai, W., et al. (2025) · The Journal of Headache and Pain · doi:10.1186/s10194-025-02210-0 · Cited by 1 · see citing works
Tuna, T., & Maren, S. (2026) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2026.1885971 · Cited by 1 · see citing works
A cortical–hippocampal communication undergoes rebalancing after new learning
Hall, A. F., & Wang, D. V. (2026) · eLife · doi:10.7554/elife.107370.3 · Cited by 1 · see citing works
A contextual fear conditioning paradigm in head-fixed mice exploring virtual realityPreprint
Krishnan, S., Dong, C., Ratigan, H. C., Morales-Rodriguez, D., Cherian, C., & Sheffield, M. E. J. (2025) · eLife · doi:10.7554/elife.105422.3 · Cited by 6 · see citing works
Self-citationThe ventral midline thalamus: Participation in neurological and neuropsychiatric disorders
Cassel, J., Panzer, É., Guimaraes-Olmo, I., Cosquer, B., de Vasconcelos, A. P., & Stéphan, A. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106315 · Cited by 1 · see citing works
A contextual fear conditioning paradigm in head-fixed mice exploring virtual realityPreprint
Krishnan, S., Dong, C., Ratigan, H. C., Morales-Rodriguez, D., Cherian, C., & Sheffield, M. E. J. (2025) · eLife · doi:10.7554/elife.105422.1 · Cited by 1 · see citing works
Self-citationA contextual fear conditioning paradigm in head-fixed mice exploring virtual realityPreprint
Krishnan, S., Dong, C., Ratigan, H. C., Morales-Rodriguez, D., Cherian, C., & Sheffield, M. E. J. (2025) · eLife · doi:10.7554/elife.105422.2 · Cited by 1 · see citing works
Self-citationMercadal, B., Guasch-Morgades, M., Mencarelli, L., Koch, G., Ruffini, G., & Initiative, A. D. N. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.09.663817 · Cited by 1 · see citing works
Furlong-Silva, J., Vere, G., Nguyen, P. T., Gotts, N., Yun Xu, A., Colombo, S. A. P., Conn, D. P., McCann, B. L., Cruz, A., Alsharq, L., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.13.664342 · Cited by 1 · see citing works
Projections from Thalamic Nucleus Reuniens to Medial Septum Enable Extinction of Remote Fear MemoryPreprint
Tomaszewski, K. F., Ziółkowska, M., Łukasiewicz, K., Cały, A., Sotoudeh, N., Puchalska, M., Salamian, A., & Radwańska, K. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4778213
CA1 Engram Cell Dynamics Before and After LearningPreprint
Ramirez, S., Monasterio, A. H., Lienkaemper, C., Coello, S., Ocker, G. K., & Scott, B. B. (2024) · Research Square · doi:10.21203/rs.3.rs-4583418/v1
Ziółkowska, M., Sotoudeh, N., Cały, A., Puchalska, M., Pagano, R., Śliwińska, M. A., Salamian, A., & Radwańska, K. (2024) · eLife · doi:10.7554/elife.101736
Ziółkowska, M., Sotoudeh, N., Cały, A., Puchalska, M., Pagano, R., Śliwińska, M. A., Salamian, A., & Radwańska, K. (2024) · eLife · doi:10.7554/elife.101736.1
A Contextual Fear Conditioning Paradigm in Head-Fixed Mice Exploring Virtual RealityPreprint
Krishnan, S., Dong, C., Ratigan, H. C., Morales-Rodriguez, D., Cherian, C., & Sheffield, M. E. J. (2024) · Qeios · doi:10.32388/ts4ate
Self-citationJohnson, G. A., Tian, Y., Hornburg, K. J., Cook, J. J., Qi, Y. P., WHITE, L. E., KILLMAR, J. T., Kaczorowski, C. C., Ashbrook, D. G., & Williams, R. W. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.08.632011
Badarnee, M., Wen, Z., Moallem, B. I., Maren, S., & Milad, M. R. (2025) · eLife · doi:10.1101/2025.07.09.663823
Sakamura, S., Suyama, K., Tsujita, A., Hsu, F.-Y., Tamada, A., Miyashita, T., Saitoe, M., Chiang, A., Inaki, M., & Matsuno, K. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.15.664853
Badarnee, M., Wen, Z., Moallem, B. I., Maren, S., & Milad, M. R. (2025) · eLife · doi:10.7554/elife.108043
Badarnee, M., Wen, Z., Moallem, B. I., Maren, S., & Milad, M. R. (2025) · eLife · doi:10.7554/elife.108043.1
A thalamo-hippocampal circuit regulating memory precision during contextual learningPreprint
Xu, C., Wu, Q., Li, Y., Chen, S., Sun, Z., Zhao, B., Huang, Y., Wang, G., Yang, M., Zhang, R., et al. (2025) · Research Square · doi:10.21203/rs.3.rs-7828569/v1
Sleep-modulated disinhibition enables replay for memory consolidation, accelerated by ripplesPreprint
Dutta, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.09.693276
Identifying distinct ensembles recruited during memory acquisition to form the engram
Pouget, C. (2024) · theses.fr (ABES) · doi:10.70675/339fe468z82fbz4f38zbe9azb44f1082d215
Li, X., Wang, H., Miao, Q., Zhou, R., He, M., Wan, H., Zhang, Y., Zhang, Q., Li, Z., Wu, Q., et al. (2026) · Diagnostics · doi:10.3390/diagnostics16081186
Theories about Cerebral Interconnections and Cognitive Functions
Kassaw, C., Olawuwo, S., & Alemayehu, S. (2026) · IntechOpen eBooks · doi:10.5772/intechopen.1014978
Farias, C. P., Leite, A. K. O., Schmidt, B. E., Júnior, O. V. R., Prauchner, G. R. K., Rieder, A. S., Teixeira, L., & Wyse, Â. T. D. S. (2026) · SSRN Electronic Journal · doi:10.2139/ssrn.6985000
Vertes, R. P., Linley, S. B., & Mitchell, A. S. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-24078-2.00014-0
Veleanu, M., Schuberth, L. E., Kilias, A., Weber, J., Warneke, J., Würz, L. M., Schwär, T., Heck, R., Müller, J., Sarrazin, D. H., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-77248-y
A cortical–hippocampal communication undergoes rebalancing after new learningPreprint
Hall, A. F., & Wang, D. V. (2026) · eLife · doi:10.7554/elife.107370.2
Badarnee, M., Wen, Z., Moallem, B. I., Maren, S., & Milad, M. R. (2026) · eLife · doi:10.7554/elife.108043.3
- Authors
- Ratigan, H. C., Krishnan, S., Smith, S., & Sheffield, M. E. J.
- Affiliations
- University of Chicago (US)
- Corresponding author
- Sheffield, Mark E. J.
- Venue
- Nature Communications
- Published
- 2023-10-24
- Volume
- 14
- Issue
- 1
- Pages
- 6758-6758
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC10598272
- OpenAlex
- W4387903600
- Cited by
- 60
- References
- 92
- Citations by year
- 2026: 12 · 2025: 28 · 2024: 17 · 2023: 3
- FWCI
- 8.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- Research Square (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion, cc-by)
- Knowledge@UChicago (University of Chicago) (submittedVersion, cc-by-nc-nd)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- University of Chicago (cc-by)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (1DP2NS111657-01)
- Whitehall Foundation
- U.S. Department of Health & Human Services | NIH | National Institute on Drug Abuse (T32DA043469)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- nucleus reuniens, hippocampal CA1, contextual fear conditioning, fear extinction, fear generalization, fear memory retrieval, fear discrimination, mice
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