Synaptic Targeting of Double-Projecting Ventral CA1 Hippocampal Neurons to the Medial Prefrontal Cortex and Basal Amygdala
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The acquisition and retrieval of contextual fear memory requires coordinated neural activity in the hippocampus, medial prefrontal cortex (mPFC), and amygdala. The contextual information encoded in the hippocampus is conveyed to the mPFC and amygdala for contextual fear conditioning. Previous studies have suggested that a CA1 neuronal population in the ventral hippocampus (VH) projects to both the mPFC and amygdala and is recruited in context-dependent control of conditioned fear. However, how double-projecting ventral CA1 hippocampal (vCA1) neurons modulate the activity of the mPFC and amygdala at the synaptic level has not been determined previously. Here, we show that the optogenetic silencing of the VH prevented the recall of contextual fear memory in mice, indicating its role in contextual fear expression. In dual retrograde viral tracing and c-Fos immunostaining experiments, we found that a proportion of vCA1 neurons projected to both the mPFC and amygdala and were recruited preferentially during context exposure, suggesting their role in encoding context representations. Moreover, optogenetic stimulation of axon collaterals of double-projecting vCA1 neurons induced monosynaptic excitatory responses in both the mPFC and basal amygdala, indicating that they could convey contextual information through the VH–mPFC and VH–amygdala pathways. The activation of double-projecting vCA1 neurons also induced action potential firings in the mPFC neurons that project to the amygdala, suggesting that they can also activate the VH–mPFC–amygdala pathway. With these synaptic mechanisms, double-projecting vCA1 neurons could induce synchronized neural activity in the mPFC and amygdala and convey contextual information efficiently to the basal amygdala for contextual fear conditioning. SIGNIFICANCE STATEMENT This work demonstrates that ventral CA1 hippocampal (vCA1) neurons projecting to both the medial prefrontal cortex (mPFC) and amygdala are activated preferentially when contextual information is processed in the ventral hippocampus, which is required for contextual fear expression. Our electrophysiological experiments reveal that the activation of double-projecting vCA1 neurons induces excitatory synaptic activity in both the mPFC and amygdala. These results suggest that double-projecting vCA1 neurons could contribute to contextual fear responses by inducing synchronized activity in the mPFC and amygdala and conveying contextual information to the basal amygdala more efficiently than vCA1 neurons projecting to either the mPFC or amygdala alone. These findings provide important insights into the mechanisms of the acquisition and retrieval of contextual fear memory.
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Inhibition of double-projecting vHPC neurons to the mPFC and basolateral amygdala interferes with contextual threat recall.
“Inhibition of double-projecting vHPC neurons to the mPFC and basolateral amygdala (BLA) interferes with contextual threat recall [42]”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [42]
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Millisecond-timescale, genetically targeted optical control of neural activity
Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., & Deisseroth, K. A. (2005) · Nature Neuroscience · doi:10.1038/nn1525 · Cited by 4,831 · see citing works
Functional organization of the hippocampal longitudinal axis
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3785 · Cited by 1,738 · 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
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
High-performance genetically targetable optical neural silencing by light-driven proton pumps
Chow, B. Y., Han, X., Dobry, A. S., Qian, X., Chuong, A. S., Li, M., Henninger, M. A., Belfort, G. M., Lin, Y., Monahan, P. E., et al. (2010) · Nature · doi:10.1038/nature08652 · Cited by 1,188 · see citing works
Pitkänen, A., Pikkarainen, M., Nurminen, N., & Ylinen, A. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06738.x · Cited by 962 · see citing works
Time cells in the hippocampus: a new dimension for mapping memories
Eichenbaum, H. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3827 · Cited by 843 · see citing works
Jay, T. M., & Witter, M. P. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903130404 · Cited by 841 · see citing works
Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat
Jung, M. W., Wiener, S. I., & McNaughton, B. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-12-07347.1994 · Cited by 818 · see citing works
Mattis, J., Tye, K. M., Ferenczi, E. A., Ramakrishnan, C., O'Shea, D. J., Prakash, R., Gunaydin, L. A., Hyun, M., Fenno, L. E., Gradinaru, V., et al. (2012) · Nature Methods · doi:10.1038/nmeth.1808 · Cited by 780 · see citing works
Finite scale of spatial representation in the hippocampus
Kjelstrup, K. B., Solstad, T., Brun, V. H., Hafting, T., Leutgeb, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2008) · Science · doi:10.1126/science.1157086 · Cited by 760 · see citing works
Ventral CA1 neurons store social memory
Okuyama, T., Kitamura, T., Roy, D. S., Itohara, S., & Tonegawa, S. (2016) · Science · doi:10.1126/science.aaf7003 · Cited by 657 · see citing works
Atasoy, D., Aponte, Y., Su, H. H., & Sternson, S. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1954-08.2008 · Cited by 614 · 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
Hippocampal Memory Traces Are Differentially Modulated by Experience, Time, and Adult Neurogenesis
Denny, C. A., Kheirbek, M. A., Alba, E. L., Tanaka, K. F., Brachman, R. A., Laughman, K. B., Tomm, N. K., Turi, G. F., Losonczy, A., & Hen, R. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.018 · Cited by 558 · 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
Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo
Maren, S., & Fanselow (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07548.1995 · Cited by 499 · see citing works
Basomedial amygdala mediates top-down control of anxiety and fear
Adhikari, A., Lerner, T. N., Finkelstein, J., Pak, S., Jennings, J. H., Davidson, T. J., Ferenczi, E., Gunaydin, L. A., Mirzabekov, J. J., Ye, L., et al. (2015) · Nature · doi:10.1038/nature15698 · Cited by 485 · see citing works
Divergent routing of positive and negative information from the amygdala during memory retrieval
Beyeler, A., Namburi, P., Glober, G. F., Simonnet, C., Calhoon, G. G., Conyers, G. F., Luck, R., Wildes, C. P., & Tye, K. M. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.004 · Cited by 412 · see citing works
Cortical Representations Are Reinstated by the Hippocampus during Memory Retrieval
Tanaka, K. Z., Pevzner, A., Hamidi, A., Nakazawa, Y., Graham, J. A., & Wiltgen, B. J. (2014) · Neuron · doi:10.1016/j.neuron.2014.09.037 · Cited by 403 · see citing works
Muller, J., Corodimas, K. P., Fridel, Z., & LeDoux, J. E. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.4.683 · Cited by 382 · cited 5× · see citing works
“…contextual fear memory Through its direct excitatory projections, the VH may regulate the neuralactivityofthemPFCandamygdala,whichisnecessaryfortherecallof contextual fear memory (Helmstetter and Bellgowan, 1994; Muller et al., 1997; Corcoran and Quirk, 2007; Goshen et al., 2011; Zhu et al., 2014).”
BackgroundInfluentialMuller, J., Corodimas, K. P., Fridel, Z., & LeDoux, J. E. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.4.683 · Cited by 382 · see citing works
Synaptic Encoding of Fear Extinction in mPFC-amygdala Circuits
Cho, J.-H., Deisseroth, K. A., & Bolshakov, V. Y. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.025 · Cited by 367 · see citing works
Self-citationSelective information routing by ventral hippocampal CA1 projection neurons
Ciocchi, S., Passecker, J., Malagon‐Vina, H., Mikuš, N., & Klausberger, T. (2015) · Science · doi:10.1126/science.aaa3245 · Cited by 344 · see citing works
Distinct Hippocampal Pathways Mediate Dissociable Roles of Context in Memory Retrieval
Xu, C., Krabbe, S., Gründemann, J., Botta, P., Fadok, J. P., Osakada, F., Saur, D., Grewe, B. F., Schnitzer, M. J., Callaway, E. M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.051 · Cited by 277 · see citing works
Lesting, J., Narayanan, R. T., Kluge, C., Sangha, S., Seidenbecher, T., & Pape, H.-C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021714 · Cited by 275 · see citing works
Helmstetter, F. J., & Bellgowan, P. S. F. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.5.1005 · Cited by 265 · see citing works
Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats
Pentkowski, N. S., Blanchard, D. C., Lever, C., Litvin, Y., & Blanchard, R. J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04754.x · Cited by 244 · see citing works
Hnasko, T. S., Perez, F. A., Scouras, A. D., Stoll, E. A., Gale, S. D., Luquet, S. H., Phillips, P. E. M., Kremer, E. J., & Palmiter, R. D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603081103 · Cited by 198 · see citing works
The ventral hippocampus and fear conditioning in rats
Bast, T., Zhang, W., & Feldon, J. (2001) · Experimental Brain Research · doi:10.1007/s002210100746 · Cited by 197 · see citing works
Trivedi, M. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.02.005 · Cited by 179 · 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 162 · see citing works
Time and Associative Learning.
Balsam, P. D., Drew, M. R., & Gallistel, C. R. (2010) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2010.50001 · Cited by 152 · see citing works
Kishi, T., Tsumori, T., Yokota, S., & Yasui, Y. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20919 · Cited by 150 · see citing works
Rudy, J. W., & Matus-Amat, P. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.154 · Cited by 147 · see citing works
Jin, J., & Maren, S. (2015) · Scientific Reports · doi:10.1038/srep08388 · Cited by 139 · see citing works
Zhang, W. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00256-x · Cited by 137 · see citing works
Ishikawa, A., & Nakamura, S. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00069.2006 · Cited by 130 · see citing works
Artificial Association of Pre-stored Information to Generate a Qualitatively New Memory
Ohkawa, N., Saitoh, Y., Suzuki, A. Z., Tsujimura, S., Murayama, E., Kosugi, S., Nishizono, H., Matsuo, M., Takahashi, Y., Nagase, M., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.03.017 · Cited by 120 · 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
Coactivation of thalamic and cortical pathways induces input timing–dependent plasticity in amygdala
Cho, J.-H., Bayazitov, I. T., Meloni, E. G., Myers, K. M., Carlezon, W. A., Zakharenko, S. S., & Bolshakov, V. Y. (2011) · Nature Neuroscience · doi:10.1038/nn.2993 · Cited by 57 · see citing works
Self-citationZhang, C.-L., Houbaert, X., Lepleux, M., Deshors, M., Normand, E., Gambino, F., Herzog, É., & Humeau, Y. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0882-x · Cited by 28 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Memory engrams: Recalling the past and imagining the future
Josselyn, S. A., & Tonegawa, S. (2020) · Science · doi:10.1126/science.aaw4325 · Cited by 1,087 · see citing works
Anxiety Cells in a Hippocampal-Hypothalamic Circuit
Jimenez, J., Su, K., Goldberg, A., Luna, V. M., Biane, J. S., Ordek, G., Zhou, P., Ong, S. K., Wright, M. A., Zweifel, L. S., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.016 · Cited by 606 · see citing works
Prefrontal cortex, amygdala, and threat processing: implications for PTSD
Alexandra Kredlow, M., Fenster, R. J., Laurent, E. S., Ressler, K. J., & Phelps, E. A. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01155-7 · Cited by 346 · see citing works
“Inhibition of double-projecting vHPC neurons to the mPFC and basolateral amygdala (BLA) interferes with contextual threat recall [42] and disconnection of the vHPC from the mPFC interferes with renewal of threat memories, a context-dependent process [43].”
BackgroundEncoding 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
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
Pentkowski, N. S., Rogge-Obando, K., Donaldson, T. N., Bouquin, S. J., & Clark, B. J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.005 · Cited by 169 · see citing works
Contextual fear memory retrieval by correlated ensembles of ventral CA1 neurons
Jimenez, J., Berry, J. E., Lim, S. C., Ong, S. K., Kheirbek, M. A., & Hen, R. (2020) · Nature Communications · doi:10.1038/s41467-020-17270-w · Cited by 157 · see citing works
Circuit and molecular architecture of a ventral hippocampal network
Gergues, M. M., Han, K. J., Choi, H. S., Brown, B., Clausing, K. J., Turner, V. S., Vainchtein, I. D., Molofsky, A. V., & Kheirbek, M. A. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0705-8 · Cited by 158 · see citing works
Pi, G., Gao, D., Wu, D., Wang, Y., Lei, H., Zeng, W., Gao, Y., Yu, H., Xiong, R., Jiang, T., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-13919-3 · Cited by 154 · see citing works
Anxiety and hippocampal neuronal activity: Relationship and potential mechanisms
Ghasemi, M., Navidhamidi, M., Rezaei, F., Azizikia, A., & Mehranfard, N. (2021) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-021-00973-y · Cited by 167 · see citing works
Hippocampus: Molecular, Cellular, and Circuit Features in Anxiety
Shi, H., Wang, S., Wang, X., Zhang, R.-X., & Zhu, L. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01020-1 · Cited by 151 · see citing works
Hippocampal-amygdala memory circuits govern experience-dependent observational fear
Terranova, J. I., Yokose, J., Osanai, H., Marks, W. D., Yamamoto, J., Ogawa, S. K., & Kitamura, T. (2022) · Neuron · doi:10.1016/j.neuron.2022.01.019 · Cited by 117 · see citing works
Liu, X., & Carter, A. G. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-18.2018 · Cited by 112 · see citing works
Neocortical synaptic engrams for remote contextual memories
Lee, J., Kim, W. B., Park, E. H., & Cho, J.-H. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01223-1 · Cited by 101 · see citing works
Self-citationBorgomaneri, S., Battaglia, S., Sciamanna, G., Tortora, F., & Laricchiuta, D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.04.036 · Cited by 90 · see citing works
Ma, L., Yue, L., Zhang, Y., Wang, Y., Han, B., Cui, S., Liu, F., Wan, Y., & Yi, M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.002 · Cited by 73 · see citing works
Arbitration of Approach-Avoidance Conflict by Ventral Hippocampus
Bryant, K. G., & Barker, J. M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.615337 · Cited by 72 · see citing works
Flexibility in the face of fear: hippocampal–prefrontal regulation of fear and avoidance
Moscarello, J. M., & Maren, S. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.09.010 · Cited by 71 · see citing works
CA2 neuronal activity controls hippocampal low gamma and ripple oscillations
Alexander, G. M., Brown, L. Y., Farris, S., Lustberg, D. J., Pantazis, C. B., Gloss, B. R., Plummer, N. W., Riddick, N. V., Moy, S. S., Jensen, P., et al. (2018) · eLife · doi:10.7554/elife.38052 · Cited by 73 · see citing works
Masurkar, A. V. (2018) · Journal of Alzheimer’s Disease & Parkinsonism · doi:10.4172/2161-0460.1000412 · Cited by 68 · see citing works
Overnight neuronal plasticity and adaptation to emotional distress
Cabrera, Y., Koymans, K. J., Poe, G. R., Kessels, H. W. H. G., Someren, E. J. W. V., & Wassing, R. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00799-w · Cited by 66 · see citing works
Ratigan, H. C., Krishnan, S., Smith, S., & Sheffield, M. E. J. (2023) · Nature Communications · doi:10.1038/s41467-023-42429-6 · Cited by 60 · see citing works
Elevation of hilar mossy cell activity suppresses hippocampal excitability and avoidance behavior
Wang, K., Wu, J., Cheng, J., Chen, C.-C., Wong, W.-Y., Averkin, R. G., Tamás, G., Nakazawa, K., & Lien, C. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109702 · Cited by 51 · see citing works
CA1 pyramidal cell diversity is rooted in the time of neurogenesis
Cavalieri, D., Angelova, A., Islah, A., Lopez, C., Bocchio, M., Bollmann, Y., Baude, A., & Cossart, R. (2021) · eLife · doi:10.7554/elife.69270 · Cited by 54 · see citing works
The Hippocampal Horizon: Constructing and Segmenting Experience for Episodic Memory
Ross, T. W., & Easton, A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.038 · Cited by 49 · see citing works
Hippocampal Inputs in the Prelimbic Cortex Curb Fear after Extinction
Szadzinska, W., Danielewski, K., Kondrakiewicz, K., Andraka, K., Nikolaev, E., Mikosz, M., & Knapska, E. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0764-20.2021 · Cited by 48 · see citing works
Twining, R. C., Lepak, K., Kirry, A. J., & Gilmartin, M. R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1453-19.2020 · Cited by 48 · see citing works
Fu, J., Yu, X.-D., Zhu, Y., Xie, S., Tang, M., Yu, B., & Li, X. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00545-z · Cited by 47 · 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 45 · see citing works
Linking external stimuli with internal drives: A role for the ventral hippocampus
Turner, V. S., O'Sullivan, R. O., & Kheirbek, M. A. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102590 · Cited by 47 · see citing works
Avoidance of learnt fear: Models, potential mechanisms, and future directions.
Wong, A. H. K., Wirth, F., & Pittig, A. (2022) · Behaviour Research and Therapy · doi:10.1016/j.brat.2022.104056 · Cited by 37 · see citing works
Riaz, S., Puveendrakumaran, P., Khan, D., Yoon, S., Hamel, L., & Ito, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-40532-7 · Cited by 40 · see citing works
Sharma, K., Kelly, E. A., Pfeifer, C. W., & Fudge, J. L. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz106 · Cited by 39 · see citing works
Alexander, G. M., Riddick, N. V., McCann, K. E., Lustberg, D. J., Moy, S. S., & Dudek, S. M. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107044 · Cited by 33 · 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
Suthard, R. L., Jellinger, A. L., Surets, M., Shpokayte, M., Pyo, A. Y., Buzharsky, M. D., Senne, R. A., Dorst, K. E., Leblanc, H., & Ramirez, S. (2022) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2023.01.007 · Cited by 33 · see citing works
Zeredo, J. L. L., Quah, S. K. L., Wallis, C. U., Alexander, L., Cockcroft, G. J., Santangelo, A. M., Xia, J., Shiba, Y., Dalley, J. W., Cardinal, R. N., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2451-18.2018 · Cited by 30 · see citing works
Dorsal Hippocampus to Infralimbic Cortex Circuit is Essential for the Recall of Extinction Memory
Qin, C., Bian, X.-L., Wu, H., Xian, J.-Y., Cai, C.-Y., Lin, Y., Zhou, Y., Kou, X., Chang, L., Luo, C., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa320 · Cited by 27 · see citing works
Patrono, E., Hrůzová, K., Svoboda, J., & Stuchlı́k, A. (2023) · Schizophrenia Research · doi:10.1016/j.schres.2022.12.047 · Cited by 28 · see citing works
Almonte, A. G., Ewin, S. E., Mauterer, M. I., Morgan, J. W., Carter, E. S., & Weiner, J. L. (2017) · Scientific Reports · doi:10.1038/s41598-017-12531-z · Cited by 26 · see citing works
Vasquez, J. H., Leong, K.-C., Gagliardi, C. M., Harland, B., Apicella, A., & Muzzio, I. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.03.003 · Cited by 29 · see citing works
The complexity of ventral CA1 and its multiple functionalities
Hong, I., & Kaang, B. (2022) · Genes Brain & Behavior · doi:10.1111/gbb.12826 · Cited by 25 · see citing works
Bozdemir, E., Vigil, F. A., Chun, S. H., Espinoza, L., Bugay, V., Khoury, S. M., Holstein, D. M., Stoja, A. P., Lozano, D., Tunca, C., et al. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01113-7 · Cited by 26 · see citing works
Soler‐Cedeño, O., Torres-Rodríguez, O. I., Bernard, F., Maldonado, L., Hernández, A., & Porter, J. T. (2019) · eNeuro · doi:10.1523/eneuro.0354-18.2019 · Cited by 25 · see citing works
Overexpression of neuropeptide Y decreases responsiveness to neuropeptide Y
Corder, K. M., Li, Q., Cortes, M. A., Bartley, A. F., Davis, T. R., & Dobrunz, L. E. (2019) · Neuropeptides · doi:10.1016/j.npep.2019.101979 · Cited by 25 · see citing works
Rahimi-Danesh, M., Samizadeh, M., Sajadi, A.-E., Rezvankhah, T., & Vaseghi, S. (2023) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2023.173675 · Cited by 26 · see citing works
Hui, C. W., Bhardwaj, S. K., Sharma, K. P., Joseph, A. T., Bisht, K., Picard, K., Tremblay, M., & Srivastava, L. K. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.12.007 · Cited by 23 · see citing works
da Costa, V. F., Ramírez, J. C. C., Ramírez, S. V., Avalo-Zuluaga, J. H., Baptista‐de‐Souza, D., Canto‐de‐Souza, L., Planeta, C. S., Rico, J. L., & Nunes‐de‐Souza, R. L. (2023) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2023.1168640 · Cited by 23 · see citing works
Coelho, A. A., Bastos, S., Gobira, P. H., & Lisboa, S. F. D. S. (2023) · Neuronal Signaling · doi:10.1042/ns20220034 · Cited by 22 · see citing works
EphB2 mediates social isolation-induced memory forgetting
Wu, X., Zhang, Y., Liu, X., Han, W.-B., Xu, N., & Sun, S. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01051-6 · Cited by 19 · see citing works
Brain‐wide mapping of presynaptic inputs to basolateral amygdala neurons
Morikawa, S., Katori, K., Takeuchi, H., & Ikegaya, Y. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25149 · Cited by 20 · see citing works
Heroux, N. A., Horgan, C. J., Pinizzotto, C. C., Rosen, J. B., & Stanton, M. E. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107091 · Cited by 18 · see citing works
Santos-Costa, N., Baptista‐de‐Souza, D., Canto‐de‐Souza, L., da Costa, V. F., & Nunes‐de‐Souza, R. L. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.695735 · Cited by 18 · see citing works
Extrafield Activity Shifts the Place Field Center of Mass to Encode Aversive Experience
Mamad, O., Agayby, B., Stumpp, L. I., Reilly, R. B., & Tsanov, M. (2019) · eNeuro · doi:10.1523/eneuro.0423-17.2019 · Cited by 18 · see citing works
Subgenual and Hippocampal Pathways in Amygdala Are Set to Balance Affect and Context Processing
Joyce, M. K. P., Wang, J., & Barbas, H. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.2066-22.2023 · Cited by 17 · see citing works
Sung, Y., & Kaang, B. (2022) · Experimental Neurobiology · doi:10.5607/en22012 · Cited by 18 · see citing works
Parallel Pathways Provide Hippocampal Spatial Information to Prefrontal Cortex
Messanvi, F., Berkun, K., Perkins, A., & Chudasama, Y. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0846-22.2022 · Cited by 15 · see citing works
Maestas-Olguin, C. R., Fennelly, J. W., & Pentkowski, N. S. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.135777 · Cited by 15 · see citing works
In it together? The case for endocannabinoid–noradrenergic interactions in fear extinction
Warren, W. G., Papagianni, E. P., Stevenson, C. W., & Stubbendorff, C. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15200 · Cited by 16 · see citing works
Extrahippocampal Seizure and Memory Circuits Overlap
Naik, A. A., Brodovskaya, A., Subedi, S., Akram, A., & Kapur, J. (2022) · eNeuro · doi:10.1523/eneuro.0179-22.2022 · Cited by 16 · see citing works
Remodeling of projections from ventral hippocampus to prefrontal cortex in Alzheimer's mice
Xu, F., Ono, M., Ito, T., Uchiumi, O., Wang, F., Zhang, Y., Sun, P., Zhang, Q., Yamaki, S., Yamamoto, R., et al. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.25032 · Cited by 15 · 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
Uzuneser, T. C., Szkudlarek, H. J., Jones, M., Nashed, M. G., Clement, T., Wang, H., Ojima, I., Rushlow, W. J., & Laviolette, S. R. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac220 · Cited by 15 · see citing works
Hippocampal area CA2 activity supports social investigation following an acute social stress
Radzicki, D., McCann, K. E., Alexander, G. M., & Dudek, S. M. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02834-9 · Cited by 15 · see citing works
A hippocampo-cortical pathway detects changes in the validity of an action as a predictor of reward
Piquet, R., Faugère, A., & Parkes, S. L. (2023) · Current Biology · doi:10.1016/j.cub.2023.11.036 · Cited by 14 · see citing works
Santarelli, A., Khan, A. M., & Poulos, A. M. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.05.015 · Cited by 15 · see citing works
Social Fear Affects Limbic System Neuronal Activity and Gene Expression
Hamann, C. S., Bankmann, J., Maza, H. M., Kornhuber, J., Zoicas, I., & Schmitt-Böhrer, A. G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158228 · Cited by 13 · see citing works
Aoki, Y., Yokoi, T., Morikawa, S., Kuga, N., Ikegaya, Y., & Sasaki, T. (2023) · iScience · doi:10.1016/j.isci.2023.107233 · Cited by 18 · see citing works
Bakoyiannis, I., Ducourneau, E., Parkes, S. L., & Ferreira, G. (2023) · Reviews in the Neurosciences · doi:10.1515/revneuro-2023-0009 · Cited by 15 · see citing works
Ma, Q., Fu, Y., Cao, Z., Shao, D., Song, J., Huan, S., Li, Y., Cui, D., Chen, M., Zhao, F., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00646 · Cited by 13 · see citing works
Minami, K., Kami, K., Nishimura, Y., Kawanishi, M., Imashiro, K., Kami, T., Habata, S., Senba, E., Umemoto, Y., & Tajima, F. (2023) · Scientific Reports · doi:10.1038/s41598-023-29849-6 · Cited by 12 · see citing works
Acute social defeat stress activated neurons project to the claustrum and basolateral amygdala
Tanuma, M., Niu, M., Ohkubo, J., Ueno, H., Nakai, Y., Yokoyama, Y., Seiriki, K., Hashimoto, H., & Kasai, A. (2022) · Molecular Brain · doi:10.1186/s13041-022-00987-8 · Cited by 11 · see citing works
Li, J., Tian, C., Yuan, S., Yin, Z., Wei, L., Chen, F., Dong, X., Liu, A., Wang, Z., Wu, T., et al. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14258 · Cited by 10 · see citing works
Bryant, K. G., Nothem, M. A., Buck, L. A., Singh, B., Amin, S., Curran‐Alfaro, C. M., & Barker, J. M. (2023) · eNeuro · doi:10.1523/eneuro.0087-23.2023 · Cited by 9 · see citing works
Hunsberger, H. C., Lee, S., Jin, M., Lanio, M., Whye, A. R., Cha, J., Scarlata, M., Matthews, L. C., Jayaseelan, K., & Denny, C. A. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.09.016 · Cited by 9 · see citing works
Mattera, A., Cavallo, A., Granato, G., Baldassarre, G., & Pagani, M. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.944838 · Cited by 10 · see citing works
Mendes, F. D. C. C. D. S., de Almeida, M. N. F., Falsoni, M., de Andrade, M. L. F., Felício, A. P. G., da Paixão, L. T. V. B., do Amaral, F. L., Anthony, D. C., Brites, D. M. T. O., Diniz, C. W. P., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116342 · Cited by 9 · see citing works
Alemán-Andrade, P., Witter, M. P., Tsutsui, K., & Ohara, S. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0217-25.2025 · Cited by 9 · see citing works
A circuit from the basolateral amygdala to hippocampal CA3 regulates social behavior
Li, M., Jiang, Y., & Sun, Q. (2025) · Current Biology · doi:10.1016/j.cub.2025.07.059 · Cited by 8 · see citing works
Amygdalostriatal transition zone neurons encode sustained cue responses to guide defensive behaviors
Mills, F., Lee, C. R., Howe, J. R., Li, H., Keisler, M. N., Shao, S., Taschbach, F., Lemieux, M., Aloboudi, F., White, J., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.08.012 · Cited by 10 · 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
Stubbendorff, C., Hale, E., Bast, T., Cassaday, H. J., Martin, S. J., Suwansawang, S., Halliday, D. M., & Stevenson, C. W. (2023) · Scientific Reports · doi:10.1038/s41598-023-44772-6 · Cited by 7 · see citing works
Origin of visual experience-dependent theta oscillations
Zimmerman, M. P., Kissinger, S. T., Edens, P. A., Towers, R. C., Nareddula, S., Nadew, Y. Y., Quinn, C. J., & Chubykin, A. A. (2024) · Current Biology · doi:10.1016/j.cub.2024.11.015 · Cited by 7 · see citing works
Bartonjo, J. J., & Lundy, R. F. (2022) · Chemical Senses · doi:10.1093/chemse/bjac009 · Cited by 7 · see citing works
Cho, H., Likhtik, E., & Dennis‐Tiwary, T. A. (2021) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-020-00855-9 · Cited by 7 · see citing works
Hippocampal-cortical interactions in the consolidation of social memory
Park, G., Kim, M. S., Lee, Y., Shin, S., Kim, S. J., Kim, S. J., Lee, Y., & Lee, Y. (2025) · Nature Communications · doi:10.1038/s41467-025-64264-7 · Cited by 6 · see citing works
Insights into the encoding of memories through the circuitry of fear
Kenna, M., Marek, R., & Sah, P. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102712 · 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
rTMS mechanisms for posttraumatic stress disorder treatment in a mouse model
Claverie, D., Cressant, A., Thomasson, J., Castellarin, C., Grandperret, V., Barbier, L., Troubat, R., Canini, F., Belzung, C., & El‐Hage, W. (2024) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2024.08.041 · Cited by 5 · see citing works
GADD45B in the ventral hippocampal CA1 modulates aversive memory acquisition and spatial cognition
Huang, M., Tao, X., Bao, J., Wang, J., Gong, X., Luo, L., Pan, S., Yang, R. Z., Gui, Y., Zhou, H., et al. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122618 · Cited by 5 · see citing works
The Role of the Hippocampus in the Perception and Recall of Odors. A Hypothetical Neural Mechanism
Silkis, I. G. (2023) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-023-01521-6 · Cited by 3 · see citing works
Hippocampal Trauma Memory Processing Conveying Susceptibility to Traumatic Stress
Dirven, B. C. J., van Melis, L. V. J., Daneva, T., Dillen, L., Homberg, J. R., Kozicz, T., & Henckens, M. J. A. G. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.01.007 · Cited by 4 · see citing works
北村, 貴., Ramesh, K., & Terranova, J. I. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-62983-9_12 · Cited by 4 · see citing works
The neural basis of affective empathy: What is known from rodents
Peng, S., Li, M., Yang, X., & Xie, W. (2025) · Neuropharmacology · doi:10.1016/j.neuropharm.2025.110347 · 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
Kim, C., Kim, S., Kim, S., Roh, J., Jin, H., & Song, B. (2020) · Brain and Behavior · doi:10.1002/brb3.1891 · Cited by 3 · see citing works
Ponce-Regalado, M. D., Salazar‐Juárez, A., Rojas-Espinosa, O., de Oca, A. C.-M., Hurtado‐Alvarado, G., Arce‐Paredes, P., Pérez‐Sánchez, G., Pavón, L., Girón‐Pérez, M. I., Hernández‐Pando, R., et al. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.03.021 · Cited by 3 · see citing works
Emotional Value of Fear Memory and the Role of the Ventral Hippocampus in Systems Consolidation
Casagrande, M. A., Porto, R. R., Haubrich, J., Kautzmann, A. S., & Alvares, L. D. O. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.11.005 · Cited by 3 · see citing works
Webster, J. F., & Cousin, M. A. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106547 · Cited by 2 · see citing works
Maladaptive learning and the amygdala—prefrontal circuit
Likhtik, E., & Paz, R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813983-7.00021-5 · Cited by 2 · see citing works
- Authors
- Kim, W. B., & Cho, J.-H.
- Affiliations
- University of California, Riverside (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2017-04-06
- Volume
- 37
- Issue
- 19
- Pages
- 4868-4882
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6596479
- OpenAlex
- W2604657615
- Cited by
- 131
- References
- 42
- Citations by year
- 2026: 12 · 2025: 10 · 2024: 10 · 2023: 23 · 2022: 17 · 2021: 20 · 2020: 16 · 2019: 11 · 2018: 9 · 2017: 3
- FWCI
- 6.12
- 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)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Centre National de la Recherche Scientifique
- University of California, Riverside
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- ventral hippocampus, medial prefrontal cortex, basal amygdala, contextual fear memory, fear conditioning, synaptic targeting, axon collaterals, optogenetic silencing, c-fos
- MeSH terms
- Animals, Avoidance Learning, Conditioning, Classical, Extinction, Psychological, Fear, Female, Male, Mice, Inbred C57BL, Neural Pathways, Neurons, Synapses, Prefrontal Cortex, CA1 Region, Hippocampal, Basolateral Nuclear Complex
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