Neural ensemble dynamics underlying a long-term associative memory
Open accessAbstract
The brain's ability to associate different stimuli is vital for long-term memory, but how neural ensembles encode associative memories is unknown. Here we studied how cell ensembles in the basal and lateral amygdala encode associations between conditioned and unconditioned stimuli (CS and US, respectively). Using a miniature fluorescence microscope, we tracked the Ca 2+ dynamics of ensembles of amygdalar neurons during fear learning and extinction over 6 days in behaving mice. Fear conditioning induced both up- and down-regulation of individual cells' CS-evoked responses. This bi-directional plasticity mainly occurred after conditioning, and reshaped the neural ensemble representation of the CS to become more similar to the US representation. During extinction training with repetitive CS presentations, the CS representation became more distinctive without reverting to its original form. Throughout the experiments, the strength of the ensemble-encoded CS-US association predicted the level of behavioural conditioning in each mouse. These findings support a supervised learning model in which activation of the US representation guides the transformation of the CS representation.
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?
The difference in response to female and male cues after the initiation of mating/fighting decreases by 40% from the initial level.
“To further explore whether mating or fighting could also induce changes in neuronal activity, we performed a Mahalanobis population vector distance (PVD) analysis (Grewe et al., 2017) and found that the difference in response to female and male cues after the initiation of mating/fighting decreases by 40% from the initial level (Figures S4C–S4F; STAR Methods).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Grewe et al., 2017
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
Ultrasensitive fluorescent proteins for imaging neuronal activity
Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., Schreiter, E. R., Kerr, R. A., Orger, M. B., Jayaraman, V., et al. (2013) · Nature · doi:10.1038/nature12354 · Cited by 6,474 · see citing works
A pyramid approach to subpixel registration based on intensity
Thévenaz, P., Ruttimann, U. E., & Unser, M. A. (1998) · IEEE Transactions on Image Processing · doi:10.1109/83.650848 · Cited by 3,097 · see citing works
The importance of mixed selectivity in complex cognitive tasks
Rigotti, M., Barak, O., Warden, M. R., Wang, X.-J., Daw, N. D., Miller, E. K., & Fusi, S. (2013) · Nature · doi:10.1038/nature12160 · Cited by 1,639 · see citing works
Neuronal signalling of fear memory
Maren, S., & Quirk, G. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1535 · Cited by 1,428 · see citing works
Long-term dynamics of CA1 hippocampal place codes
Ziv, Y., Burns, L. D., Cocker, E. D., Hamel, E. O., Ghosh, K. K., Kitch, L. J., Gamal, A. E., & Schnitzer, M. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3329 · Cited by 1,155 · see citing works
Miniaturized integration of a fluorescence microscope
Ghosh, K. K., Burns, L. D., Cocker, E. D., Nimmerjahn, A., Ziv, Y., Gamal, A. E., & Schnitzer, M. J. (2011) · Nature Methods · doi:10.1038/nmeth.1694 · Cited by 1,130 · see citing works
Switching on and off fear by distinct neuronal circuits
Herry, C., Ciocchi, S., Senn, V., Demmou, L., Müller, C., & Lüthi, A. (2008) · Nature · doi:10.1038/nature07166 · Cited by 950 · see citing works
Encoding of conditioned fear in central amygdala inhibitory circuits
Ciocchi, S., Herry, C., Grenier, F., Wolff, S. B. E., Letzkus, J. J., Vlachos, I., Ehrlich, I., Sprengel, R., Deisseroth, K., Stadler, M. B., et al. (2010) · Nature · doi:10.1038/nature09559 · Cited by 924 · see citing works
The primate amygdala represents the positive and negative value of visual stimuli during learning
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006) · Nature · doi:10.1038/nature04490 · Cited by 917 · see citing works
Quirk, G. J., Repa, J. C., & LeDoux, J. E. (1995) · Neuron · doi:10.1016/0896-6273(95)90092-6 · Cited by 808 · see citing works
The tempotron: a neuron that learns spike timing–based decisions
Gütig, R., & Sompolinsky, H. (2006) · Nature Neuroscience · doi:10.1038/nn1643 · Cited by 805 · see citing works
Postsynaptic receptor trafficking underlying a form of associative learning
Rumpel, S., LeDoux, J., Zador, A., & Malinow, R. (2005) · Science · doi:10.1126/science.1103944 · Cited by 775 · see citing works
Automated Analysis of Cellular Signals from Large-Scale Calcium Imaging Data
Mukamel, E. A., Nimmerjahn, A., & Schnitzer, M. J. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.009 · Cited by 711 · see citing works
Neurons for hunger and thirst transmit a negative-valence teaching signal
Betley, J. N., Xu, S., Cao, Z. F. H., Gong, R., Magnus, C. J., Yu, Y., & Sternson, S. M. (2015) · Nature · doi:10.1038/nature14416 · Cited by 704 · see citing works
Neuronal competition and selection during memory formation
Han, J.-H., Kushner, S. A., Yiu, A. P., Cole, C. J., Matynia, A., Brown, R. A., Neve, R. L., Guzowski, J. F., Silva, A. J., & Josselyn, S. A. (2007) · Science · doi:10.1126/science.1139438 · Cited by 682 · see citing works
Prefrontal control of fear: more than just extinction
Sotres-Bayon, F., & Quirk, G. J. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.005 · Cited by 625 · see citing works
A circuit mechanism for differentiating positive and negative associations
Namburi, P., Beyeler, A., Yorozu, S., Calhoon, G. G., Halbert, S. A., Wichmann, R., Holden, S. S., Mertens, K. L., Anahtar, M., Felix-Ortiz, A. C., et al. (2015) · Nature · doi:10.1038/nature14366 · Cited by 614 · see citing works
Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning
Blair, H. T., Schafe, G. E., Bauer, E. P., Rodrigues, S. M., & LeDoux, J. E. (2001) · Learning & Memory · doi:10.1101/lm.30901 · Cited by 610 · see citing works
Quirk, G. J., Armony, J. L., & LeDoux, J. E. (1997) · Neuron · doi:10.1016/s0896-6273(00)80375-x · Cited by 563 · 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 · see citing works
Molecular mechanisms underlying emotional learning and memory in the lateral amygdala
Rodrigues, S. M., Schafe, G. E., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.014 · Cited by 491 · see citing works
Amygdala interneuron subtypes control fear learning through disinhibition
Wolff, S. B. E., Gründemann, J., Tovote, P., Krabbe, S., Jacobson, G. A., Müller, C. R., Herry, C., Ehrlich, I., Friedrich, R. W., Letzkus, J. J., et al. (2014) · Nature · doi:10.1038/nature13258 · Cited by 489 · see citing works
Somatosensory and auditory convergence in the lateral nucleus of the amygdala.
Romanski, L. M., Clugnet, M.-C., Bordi, F., & LeDoux, J. E. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.3.444 · Cited by 446 · see citing works
Competition between engrams influences fear memory formation and recall
Rashid, A. J., Chen, Y., Mercaldo, V., Hsiang, H., Park, S., Cole, C. J., Cristofaro, A. D., Yu, J., Ramakrishnan, C., Lee, S. Y., et al. (2016) · Science · doi:10.1126/science.aaf0594 · Cited by 424 · see citing works
Neuromodulated Spike-Timing-Dependent Plasticity, and Theory of Three-Factor Learning Rules
Frémaux, N., & Gerstner, W. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00085 · Cited by 404 · see citing works
Generation of a synthetic memory trace
Garner, A. R., Rowland, D. C., Hwang, S. Y., Baumgaertel, K., Roth, B. L., Kentros, C., & Mayford, M. (2012) · Science · doi:10.1126/science.1214985 · Cited by 387 · see citing works
Neuronal code for extended time in the hippocampus
Mankin, E. A., Sparks, F. T., Slayyeh, B., Sutherland, R. J., Leutgeb, S., & Leutgeb, J. K. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214107109 · Cited by 371 · see citing works
Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala
Belova, M. A., Paton, J. J., Morrison, S. E., & Salzman, C. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.004 · Cited by 349 · see citing works
Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray
Johansen, J. P., Tarpley, J. W., LeDoux, J. E., & Blair, H. T. (2010) · Nature Neuroscience · doi:10.1038/nn.2594 · Cited by 312 · see citing works
Sublayer-Specific Coding Dynamics during Spatial Navigation and Learning in Hippocampal Area CA1
Danielson, N. B., Zaremba, J. D., Kaifosh, P., Bowler, J., Ladow, M., & Losonczy, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.020 · Cited by 288 · see citing works
Hippocampal ensemble dynamics timestamp events in long-term memory
Rubin, A., Geva, N., Sheintuch, L., & Ziv, Y. (2015) · eLife · doi:10.7554/elife.12247 · Cited by 266 · see citing works
Gore, F., Schwartz, E. C., Brangers, B. C., Aladi, S., Stujenske, J. M., Likhtik, E., Russo, M. J., Gordon, J. A., Salzman, C. D., & Axel, R. (2015) · Cell · doi:10.1016/j.cell.2015.06.027 · Cited by 256 · see citing works
Timing is not everything: neuromodulation opens the STDP gate
Pawlak, V. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00146 · Cited by 254 · see citing works
Dopamine is necessary for cue-dependent fear conditioning
Fadok, J. P., Dickerson, T. M. K., & Palmiter, R. D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1616-09.2009 · Cited by 213 · see citing works
Maren, S., Yap, S. A., & Goosens, K. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-06-j0001.2001 · Cited by 186 · see citing works
Hebbian and neuromodulatory mechanisms interact to trigger associative memory formation
Johansen, J. P., Díaz-Mataix, L., Hamanaka, H., Ozawa, T., Ycu, E. A., Koivumaa, J., Kumar, A., Hou, M., Deisseroth, K. A., Boyden, E. S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421304111 · Cited by 179 · see citing works
Chowdhury, N., Quinn, J. J., & Fanselow, M. S. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.5.1396 · Cited by 160 · see citing works
Sah, P., Westbrook, R. F., & Lüthi, A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1417.020 · Cited by 138 · see citing works
Self-citationAuditory-Evoked Spike Firing in the Lateral Amygdala and Pavlovian Fear Conditioning
Goosens, K. A., Hobin, J. A., & Maren, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00728-1 · Cited by 135 · see citing works
Learning not to Fear: Neural Correlates of Learned Safety
Kong, E., Monje, F. J., Hirsch, J., & Pollak, D. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.191 · Cited by 113 · see citing works
Double Dissociation of Amygdala and Hippocampal Contributions to Trace and Delay Fear Conditioning
Raybuck, J. D., & Lattal, K. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015982 · Cited by 105 · see citing works
Singeç, I., Knoth, R., Ditter, M., Volk, B., & Frotscher, M. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20302 · Cited by 63 · see citing works
Unilateral Storage of Fear Memories by the Amygdala
Blair, H. T., Huynh, V. K., Vaz, V. T., Van, J., Patel, R. R., Hiteshi, A. K., Lee, J. E., & Tarpley, J. W. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0674-05.2005 · Cited by 43 · see citing works
Erlich, J. C., Bush, D. E. A., & LeDoux, J. E. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00016 · Cited by 40 · see citing works
Molecular and Cellular Mechanisms for Trapping and Activating Emotional Memories
Rogerson, T., Jayaprakash, B., Cai, D. J., Sano, Y., Lee, Y., Zhou, Y., Bekal, P., Deisseroth, K. A., & Silva, A. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161655 · Cited by 31 · see citing works
The ups and downs of Hebb synapses.
Hinton, G. E. (2003) · Canadian Psychology/Psychologie canadienne · doi:10.1037/h0085812 · Cited by 22 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [21]Bishop CM Pattern Recognition and Machine Learning 2007 1 Springer
Cited by
Sorted by citations
What Is a Cognitive Map? Organizing Knowledge for Flexible Behavior
Behrens, T. E. J., Muller, T. H., Whittington, J. C. R., Mark, S., Baram, A. B., Stachenfeld, K. L., & Kurth-Nelson, Z. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.002 · Cited by 1,055 · see citing works
Temporal evolution of cortical ensembles promoting remote memory retrieval
DeNardo, L. A., Liu, C. D., Allen, W. E., Adams, E. L., Friedmann, D., Dadgar‐Kiani, E., Fu, L., Guenthner, C. J., Lee, J. H., Tessier‐Lavigne, M., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0318-7 · Cited by 615 · see citing works
Neural circuit mechanisms of social behavior
Chen, P., & Hong, W. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.026 · Cited by 527 · see citing works
Genetic Dissection of Neural Circuits: A Decade of Progress
Luo, L., Callaway, E. M., & Svoboda, K. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.040 · Cited by 446 · see citing works
An amygdalar neural ensemble that encodes the unpleasantness of pain
Corder, G. F., Ahanonu, B., Grewe, B. F., Wang, D., Schnitzer, M. J., & Scherrer, G. (2019) · Science · doi:10.1126/science.aap8586 · Cited by 406 · see citing works
Tracking the Same Neurons across Multiple Days in Ca2+ Imaging Data
Sheintuch, L., Rubin, A., Brande-Eilat, N., Geva, N., Sadeh, N., Pinchasof, O., & Ziv, Y. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.013 · Cited by 394 · see citing works
“Thus, the set of detected cells can differ between sessions (Ziv et al., 2013; Resendez et al., 2016; Grewe et al., 2017; Xia et al., 2017), and a one-toone mapping of neural identity across sessions is typically not attainable.”
BackgroundDistinct 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
Williams, A. H., Kim, T. H., Wang, F. L., Vyas, S., Ryu, S. I., Shenoy, K. V., Schnitzer, M. J., Kolda, T. G., & Ganguli, S. (2018) · Neuron · doi:10.1016/j.neuron.2018.05.015 · Cited by 306 · see citing works
Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice
Li, Y., Mathis, A., Grewe, B. F., Osterhout, J. A., Ahanonu, B., Schnitzer, M. J., Murthy, V. N., & Dulac, C. (2017) · Cell · doi:10.1016/j.cell.2017.10.015 · Cited by 291 · see citing works
“…Cellsort MATLAB algorithm for extracting cellular Ca2+ signals Ziv et al., 2013 N/A Registration of cell identities across imaging sessions Grewe et al., 2017 N/A Fast nonnegative deconvolution Vogelstein et al., 2010 N/A Other 0.85-mm custom GRIN lens Grintech…”
InfluentialAmygdala Reward Neurons Form and Store Fear Extinction Memory
Zhang, X., Kim, J., & Tonegawa, S. (2019) · Neuron · doi:10.1016/j.neuron.2019.12.025 · Cited by 279 · see citing works
Functionally Distinct Neuronal Ensembles within the Memory Engram
Sun, X., Bernstein, M. J., Meng, M., Rao, S., Sørensen, A. T., Yao, L., Zhang, X., Anikeeva, P., & Lin, Y. (2020) · Cell · doi:10.1016/j.cell.2020.02.055 · Cited by 270 · see citing works
Amygdala Inhibitory Circuits Regulate Associative Fear Conditioning
Krabbe, S., Gründemann, J., & Lüthi, A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.006 · Cited by 255 · see citing works
“Conclusions and future directions The increasing numbers of cell type-specific genetically modified mouse lines, together with technical advances in optogenetics as well as tracing and recording techniques have led to major progress in understanding the role of defined inhibitory microcircuits in the amygdala (31; 33;…”
BackgroundInfluentialCentral amygdala circuits modulate food consumption through a positive-valence mechanism
Douglass, A. M., Kucukdereli, H., Ponserre, M., Marković, M., Gründemann, J., Strobel, C., Morales, P. L. A., Conzelmann, K., Lüthi, A., & Klein, R. (2017) · Nature Neuroscience · doi:10.1038/nn.4623 · Cited by 257 · see citing works
Estimation of Current and Future Physiological States in Insular Cortex
Livneh, Y., Sugden, A. U., Madara, J. C., Essner, R. A., Flores, V. I., Sugden, L. A., Resch, J. M., Lowell, B. B., & Andermann, M. L. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.027 · Cited by 209 · see citing works
Brain circuits for pain and its treatment
Lindsay, N. M., Chen, C., Gilam, G., Mackey, S., & Scherrer, G. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abj7360 · Cited by 234 · see citing works
Amygdala ensembles encode behavioral states
Gründemann, J., Bitterman, Y., Lu, T., Krabbe, S., Grewe, B. F., Schnitzer, M. J., & Lüthi, A. (2019) · Science · doi:10.1126/science.aav8736 · Cited by 223 · see citing works
Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex
Remedios, R., Kennedy, A., Zelikowsky, M., Grewe, B. F., Schnitzer, M. J., & Anderson, D. J. (2017) · Nature · doi:10.1038/nature23885 · Cited by 218 · see citing works
Integration of Parallel Opposing Memories Underlies Memory Extinction
Felsenberg, J., Jacob, P. F., Walker, T. M., Barnstedt, O., Edmondson-Stait, A. J., Pleijzier, M. W., Otto, N., Schlegel, P., Sharifi, N., Perisse, E., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.021 · Cited by 217 · see citing works
“Perhaps an analogous arrangement of parallel competing memories (Grewe et al., 2017), driven by teaching signals (Saunders et al.”
BackgroundWireless optoelectronic photometers for monitoring neuronal dynamics in the deep brain
Lu, L., Gutruf, P., Li, X., Bhatti, D. L., Wang, X., Vázquez‐Guardado, A., Ning, X., Shen, X., Sang, T., Ma, R., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1718721115 · Cited by 205 · see citing works
State-specific gating of salient cues by midbrain dopaminergic input to basal amygdala
Lutas, A., Kucukdereli, H., Alturkistani, O., Carty, C., Sugden, A. U., Fernando, K., Diaz, V. E., Flores-Maldonado, V., & Andermann, M. L. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0506-0 · Cited by 166 · see citing works
Adaptive disinhibitory gating by VIP interneurons permits associative learning
Krabbe, S., Paradiso, E., d‘Aquin, S., Bitterman, Y., Courtin, J., Xu, C., Yonehara, K., Marković, M., Müller, C. R., Eichlisberger, T., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0508-y · Cited by 161 · see citing works
Fluorescence imaging of large-scale neural ensemble dynamics
Kim, T. H., & Schnitzer, M. J. (2022) · Cell · doi:10.1016/j.cell.2021.12.007 · Cited by 165 · see citing works
“Notably, bilateral implants within the same brain structure may increase the risk of behavioral deficits (Grewe et al., 2017).”
BackgroundOrchestrated 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
Namboodiri, V. M. K., Otis, J. M., van Heeswijk, K., Voets, E. S., Alghorazi, R. A., Rodriguez-Romaguera, J., Mihalas, S., & Stuber, G. D. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0408-1 · Cited by 150 · see citing works
MIN1PIPE: A Miniscope 1-Photon-Based Calcium Imaging Signal Extraction Pipeline
Lu, J., Li, C., Alvarado, J. S., Zhou, Z., Frӧhlich, F., MOONEY, R. D., & Wang, F. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.062 · Cited by 155 · see citing works
Kumar, D., Koyanagi, I., Carrier‐Ruiz, A., Vergara, P., Srinivasan, S., Sugaya, Y., Kasuya, M., Yu, T., Vogt, K. E., Muratani, M., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.008 · Cited by 144 · see citing works
Multi-dimensional coding by basolateral amygdala neurons
Kyriazi, P., Headley, D. B., & Pare, D. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.036 · Cited by 130 · see citing works
Basolateral amygdala circuitry in positive and negative valence
O’Neill, P.-K., Gore, F., & Salzman, C. D. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.012 · Cited by 139 · see citing works
Fear, Anxiety, and the Amygdala
Sah, P. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.013 · Cited by 137 · see citing works
“A reduction in activity in the BLA by the conditioned aversive CS has also recently been reported using calcium imaging (Grewe et al., 2017).”
MethodPrecision Calcium Imaging of Dense Neural Populations via a Cell-Body-Targeted Calcium Indicator
Shemesh, O. A., Linghu, C., Piatkevich, K. D., Goodwin, D., Celiker, O. T., Gritton, H. J., Romano, M. F., Gao, R., Yu, C.-C., Tseng, H.-A., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.029 · Cited by 137 · see citing works
The brain in motion: How ensemble fluidity drives memory-updating and flexibility
Mau, W., Hasselmo, M. E., & Cai, D. J. (2020) · eLife · doi:10.7554/elife.63550 · Cited by 139 · see citing works
Synaptic encoding of fear memories in the amygdala
Ressler, R. L., & Maren, S. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.08.012 · Cited by 132 · see citing works
Population coding of valence in the basolateral amygdala
Zhang, X., & Li, B. (2018) · Nature Communications · doi:10.1038/s41467-018-07679-9 · Cited by 133 · see citing works
Tang, W., Kochubey, O., Kintscher, M., & Schneggenburger, R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1796-19.2020 · Cited by 123 · see citing works
“Tone (CS)driven action potential (AP) firing is increased in many lateral amygdala (LA) and basal amygdala (BA) neurons during and after fear conditioning protocols (Quirk et al., 1995; Amano et al., 2011; Grewe et al., 2017).”
BackgroundIntercalated amygdala clusters orchestrate a switch in fear state
Hagihara, K. M., Bukalo, O., Zeller, M., Aksoy‐Aksel, A., Karalis, N., Limoges, A., Rigg, T., Campbell, T. L., Mendez, A., Weinholtz, C. A., et al. (2021) · Nature · doi:10.1038/s41586-021-03593-1 · Cited by 113 · see citing works
Bienvenu, T., Déjean, C., Jercog, D., Aouizerate, B., Lemoine, M., & Herry, C. (2021) · Neuron · doi:10.1016/j.neuron.2021.05.017 · Cited by 107 · see citing works
Rewiring the connectome: Evidence and effects
Bennett, S. H., Kirby, A. J., & Finnerty, G. T. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.03.001 · Cited by 104 · see citing works
Expectation-induced modulation of metastable activity underlies faster coding of sensory stimuli
Mazzucato, L., Camera, G. L., Fontanini, A., Alfredo, F., & Giancarlo, L. C. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0364-9 · Cited by 97 · see citing works
Besnard, A., Gao, Y., Kim, M. T., Twarkowski, H., Reed, A. K., Langberg, T., Feng, W., Xu, X., Saur, D., Zweifel, L. S., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0330-y · Cited by 94 · see citing works
Fear conditioning and the basolateral amygdala
Sun, Y., Gooch, H., & Sah, P. (2020) · F1000Research · doi:10.12688/f1000research.21201.1 · Cited by 104 · see citing works
A Critical Role for Neocortical Processing of Threat Memory
Dalmay, T., Abs, E., Poorthuis, R. B., Hartung, J., Pu, D.-L., Onasch, S., Lozano, Y. R., Signoret-Genest, J., Tovote, P., Gjorgjieva, J., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.025 · Cited by 88 · see citing works
Characterizing Cortex-Wide Dynamics with Wide-Field Calcium Imaging
Ren, C., & Komiyama, T. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.3003-20.2021 · Cited by 86 · see citing works
“Learning-related dynamics in macroscopic cortical activity Learning-induced plasticity has been under intense scrutiny with electrophysiological recordings and two-photon calcium imaging (Costa et al., 2004; Peters et al., 2014; Makino and Komiyama, 2015; Grewe et al., 2017).”
BackgroundHippocampal Network Reorganization Underlies the Formation of a Temporal Association Memory
Ahmed, M. S., Priestley, J. B., Castro, A., Stefanini, F., Canales, A. S. S., Balough, E. M., Lavoie, E., Mazzucato, L., Fusi, S., & Losonczy, A. (2020) · Neuron · doi:10.1016/j.neuron.2020.04.013 · Cited by 86 · see citing works
Differential Recruitment of Competing Valence-Related Amygdala Networks during Anxiety
Lee, S., Amir, A., Haufler, D., & Paré, D. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.002 · Cited by 87 · see citing works
“Similarly, bi-directional changes in CS-induced Ca2+ responses were observed in LA after fear conditioning (Grewe et al., 2017), indicating that learning produces bidirectional changes in neural activity in the amygdala.”
A Compact Head‐Mounted Endoscope for In Vivo Calcium Imaging in Freely Behaving Mice
Jacob, A. D., Ramsaran, A. I., Mocle, A. J., Tran, L. M., Yan, C., Frankland, P. W., & Josselyn, S. A. (2018) · Current Protocols in Neuroscience · doi:10.1002/cpns.51 · Cited by 82 · see citing works
Trott, J. M., Hoffman, A. N., Zhuravka, I., & Fanselow, M. S. (2022) · eLife · doi:10.7554/elife.75663 · Cited by 84 · see citing works
Kayyal, H., Yiannakas, A., Chandran, S. K., Khamaisy, M., Sharma, V. K., & Rosenblum, K. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0752-19.2019 · Cited by 80 · see citing works
The Computational and Neural Bases of Context-Dependent Learning
Heald, J. B., Wolpert, D. M., & Lengyel, M. (2023) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-092322-100402 · Cited by 84 · see citing works
Associative and plastic thalamic signaling to the lateral amygdala controls fear behavior
Barsy, B., Kocsis, K., Magyar, A., Babiczky, Á., Szabó, M., Veres, J. M., Hillier, D., Ulbert, I., Yizhar, O., & Mátyás, F. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0620-z · Cited by 77 · see citing works
Modulation of Ion Channels in the Axon: Mechanisms and Function
Burke, K. J., & Bender, K. J. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00221 · Cited by 75 · see citing works
Bombesin-Like Peptide Recruits Disinhibitory Cortical Circuits and Enhances Fear Memories
Melzer, S., Newmark, E., Mizuno, G. O., Hyun, M., Philson, A. C., Quiroli, E., Righetti, B., Gregory, M. R., Huang, K. W., Levasseur, J., et al. (2020) · Cell · doi:10.1016/j.cell.2021.09.013 · Cited by 78 · see citing works
Zhang, W., Liu, W.-Z., He, Y., You, W.-J., Zhang, J., Xu, H. A., Tian, X.-L., Li, B., Mei, L., Holmes, A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.12.010 · Cited by 72 · see citing works
Wen, Z., Raio, C. M., Pace-Schott, E. F., Lazar, S. W., LeDoux, J. E., Phelps, E. A., & Milad, M. R. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204066119 · Cited by 69 · see citing works
Basolateral Amygdala Neurons Maintain Aversive Emotional Salience
Sengupta, A., Yau, J. O.-Y., Jean-Richard-dit-Bressel, P., Liu, Y., Millan, E. Z., Power, J., & McNally, G. P. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2460-17.2017 · Cited by 71 · see citing works
“Interestingly, our photometry data showed no evidence, at the population level, for changes in US-evoked activity (but for one example of such decreases in single-unit activity, see Johansen et al., 2010b; for examples of increases and decreases, see Grewe et al., 2017).”
BackgroundCorticocortical Systems Underlying High-Order Motor Control
Battaglia‐Mayer, A., & Caminiti, R. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2094-18.2019 · Cited by 72 · see citing works
“, 2017), hippocampal memory formation (Grewe et al., 2017) and communication with the amygdala (Xu et al.”
BackgroundInhibitory microcircuits for top-down plasticity of sensory representations
Wilmes, K. A., & Claudia Clopath, A. (2019) · Nature Communications · doi:10.1038/s41467-019-12972-2 · Cited by 69 · see citing works
Sità, L., Brondi, M., Roig, P. L. D. L., Curreli, S., Panniello, M., Vecchia, D., & Fellin, T. (2022) · Nature Communications · doi:10.1038/s41467-022-29180-0 · Cited by 67 · see citing works
Nucleus accumbens fast-spiking interneurons in motivational and addictive behaviors
Schall, T. A., Wright, W. J., & Dong, Y. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0683-y · Cited by 62 · see citing works
Robert, B., Kimchi, E. Y., Watanabe, Y., Chakoma, T. L., Jing, M., Li, Y., & Polley, D. B. (2021) · eLife · doi:10.7554/elife.69514 · Cited by 64 · see citing works
Piantadosi, S. C., Zhou, Z. C., Pizzano, C., Pedersen, C. E., Nguyen, T. K., Thai, S., Stuber, G. D., & Bruchas, M. R. (2023) · Neuron · doi:10.1016/j.neuron.2023.11.007 · Cited by 64 · see citing works
Intermingled Ensembles in Visual Association Cortex Encode Stimulus Identity or Predicted Outcome
Ramesh, R. N., Burgess, C. R., Sugden, A. U., Gyetvan, M., & Andermann, M. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.024 · Cited by 64 · see citing works
Compartmentalized dendritic plasticity during associative learning
d‘Aquin, S., Szőnyi, A., Mahn, M., Krabbe, S., Gründemann, J., & Lüthi, A. (2022) · Science · doi:10.1126/science.abf7052 · Cited by 60 · see citing works
“S7I), which suggests that updating of CS response representations is necessary for conditioned freezing behavior (21).”
BackgroundResultInfluentialPastor‐Bernier, A., Stasiak, A., & Schultz, W. (2019) · Nature Communications · doi:10.1038/s41467-019-12792-4 · Cited by 61 · see citing works
Taylor, J. A., Hasegawa, M., Benoit, C. M., Freire, J. A., Théodore, M., Ganea, D. A., Innocenti, S. M., Lu, T., & Gründemann, J. (2021) · Nature Communications · doi:10.1038/s41467-021-22421-8 · Cited by 63 · see citing works
“Nevertheless, the transient population level changes during fear conditioning in MGB might be crucial to guide long term population level changes in the amygdala or other downstream areas upon associative learning (Chen et al., 2019; Grewe et al., 2017; Zhang and Li, 2018).”
BackgroundMethodResultInfluentialLost in translation: How to upgrade fear memory research
Flores, Á., Fullana, M. À., Soriano-Mas, C., & Andero, R. (2018) · Molecular Psychiatry · doi:10.1038/s41380-017-0006-0 · Cited by 59 · see citing works
“In fact, a recent work employing an intracellular calcium indicator to characterize the dynamics of amygdalar ensembles during FC and extinction has revealed a learning model that may have been unapparent in smaller recordings [60].”
BackgroundO’Mara, S. M., & Aggleton, J. P. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00052 · Cited by 59 · see citing works
“Subsequent demonstrations that pharmacological inhibitors of hippocampal LTP effectively inhibited learning and memory in spatial memory tasks, have also provided a rich source of theory and experiment focused on the role of the hippocampal formation in learning and memory (e.g., Bliss and Collingridge, 1993; van Praa…”
BackgroundNeural substrates of appetitive and aversive prediction error
Iordanova, M. D., Yau, J. O.-Y., McDannald, M. A., & Corbit, L. H. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.029 · Cited by 60 · see citing works
“Most importantly, this outcome-evoked BLA activity is necessary for learning because silencing BLA PNs at the time of shock during fear conditioning impaireds learning (Namburi et al., 2015; Sengupta et al., 2018; Wolff et al., 2014) whereas excitation of BLA PNs during shock outcome facilitates learning (Johansen et…”
BackgroundInfluentialEmbracing Complexity in Defensive Networks
Headley, D. B., Kanta, V., Kyriazi, P., & Paré, D. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.024 · Cited by 53 · see citing works
“In mice trained to associate a tone CS with a shock US, the CS coding ensemble became more similar to the US ensemble (Grewe et al., 2017).”
BackgroundInfluentialThe essence of the engram: Cellular or synaptic?
Han, D. H., Park, P., Choi, D. I., Bliss, T., & Kaang, B. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.033 · Cited by 53 · see citing works
Qin, S., Farashahi, S. G., Lipshutz, D., Sengupta, A. M., Chklovskii, D. B., & Pehlevan, C. (2023) · Nature Neuroscience · doi:10.1038/s41593-022-01225-z · Cited by 61 · see citing works
“The neural ensemble representation of conditional stimuli in mouse amygdala shows continuous change over days after fear conditioning 16 .”
BackgroundValue generalization in human avoidance learning
Norbury, A., Robbins, T. W., & Seymour, B. (2018) · eLife · doi:10.7554/elife.34779 · Cited by 54 · see citing works
“In previous studies of Pavlovian aversive conditioning, it has been demonstrated that positively conditioned stimuli come to be more closely represented to the primary aversive outcome in multivariate space (e.g. across neural ensemble activity in the basolateral amygdala, Grewe et al., 2017).”
BackgroundInfluentialThe mysteries of remote memory
Albo, Z., & Gräff, J. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0029 · Cited by 53 · see citing works
Leveraging calcium imaging to illuminate circuit dysfunction in addiction
Siciliano, C. A., & Tye, K. M. (2019) · Alcohol · doi:10.1016/j.alcohol.2018.05.013 · Cited by 53 · see citing works
Projection from the Amygdala to the Thalamic Reticular Nucleus Amplifies Cortical Sound Responses
Aizenberg, M., Rolón‐Martínez, S., Pham, T. D., Rao, W., Haas, J. S., & Geffen, M. N. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.050 · Cited by 52 · see citing works
Heterogeneous Habenular Neuronal Ensembles during Selection of Defensive Behaviors
Lecca, S., Namboodiri, V. M. K., Restivo, L., Gervasi, N., Pillolla, G., Stuber, G. D., & Mameli, M. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107752 · Cited by 52 · see citing works
Circuit reorganization in the Drosophila mushroom body calyx accompanies memory consolidation
Baltruschat, L., Prisco, L., Ranft, P., Lauritzen, J. S., Fiala, A., Bock, D. D., & Tavosanis, G. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108871 · Cited by 52 · see citing works
Jo, Y. S., Namboodiri, V. M. K., Stuber, G. D., & Zweifel, L. S. (2020) · Nature Communications · doi:10.1038/s41467-020-14393-y · Cited by 53 · 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
“Recent work showed that during conditioning, BLA principal neurons (PNs) remap to encode fear-conditioned stimuli, whereas neutral stimuli remain passively maintained (Grewe et al., 2017).”
Hippocampal Hyperactivity as a Druggable Circuit-Level Origin of Aberrant Salience in Schizophrenia
Kätzel, D., Wolff, A. R., Bygrave, A. M., & Bannerman, D. M. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.486811 · Cited by 50 · see citing works
Aschauer, D. F., Eppler, J.-B., Ewig, L., Chambers, A. R., Pokorny, C., Kaschube, M., & Rumpel, S. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110340 · Cited by 48 · see citing works
Dunn, A. R., & Kaczorowski, C. C. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107069 · Cited by 42 · see citing works
Hippocampus and amygdala fear memory engrams re-emerge after contextual fear relapse
Zaki, Y., Mau, W., Cincotta, C., Monasterio, A., Odom, E. I., Doucette, E., Grella, S. L., Merfeld, E., Shpokayte, M., & Ramirez, S. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01407-0 · Cited by 49 · see citing works
“We found that over EXT, the population states in the BLA and CA1 followed a trajectory that gradually deviated from its CFC state, supporting the idea of a network-wide transformation over extinction [33, 36, 43, 44] (Fig.”
BackgroundAssociative memory cells and their working principle in the brain
Wang, J., & Cui, S. (2018) · F1000Research · doi:10.12688/f1000research.13665.1 · Cited by 46 · see citing works
A Probabilistic Framework for Decoding Behavior From in vivo Calcium Imaging Data
Etter, G., Manseau, F., & Williams, S. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.00019 · Cited by 45 · see citing works
Fast varifocal two-photon microendoscope for imaging neuronal activity in the deep brain
Sato, M., Motegi, Y., Yagi, S., Gengyo‐Ando, K., Ohkura, M., & Nakai, J. (2017) · Biomedical Optics Express · doi:10.1364/boe.8.004049 · Cited by 43 · see citing works
The dynamic nature of fear engrams in the basolateral amygdala
Davis, P. W., & Reijmers, L. G. J. E. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.12.004 · Cited by 41 · see citing works
“These miniscopes have recently been used for the longitudinal imaging of neural activity patterns in the BLA during cued fear memory encoding, extinction, and retrieval (Grewe et al., 2017).”
MethodBerret, E., Kintscher, M., Palchaudhuri, S., Tang, W., Osypenko, D., Kochubey, O., & Schneggenburger, R. (2019) · Science · doi:10.1126/science.aaw0474 · Cited by 40 · see citing works
RetractedDistinct ventral hippocampal inhibitory microcircuits regulating anxiety and fear behaviors
Li, K., Koukoutselos, K., Sakaguchi, M., & Ciocchi, S. (2024) · Nature Communications · doi:10.1038/s41467-024-52466-4 · Cited by 41 · see citing works
A neural mechanism for learning from delayed postingestive feedback
Zimmerman, C. A., Bolkan, S. S., Pan-Vazquez, A., Wu, B., Keppler, E., Meares-Garcia, J. B., Guthman, E. M., Fetcho, R. N., McMannon, B., Lee, J., et al. (2025) · Nature · doi:10.1038/s41586-025-08828-z · Cited by 42 · see citing works
Instrumental aversion coding in the basolateral amygdala and its reversion by a benzodiazepine
Jean-Richard-dit-Bressel, P., Tran, J., Didachos, A., & McNally, G. P. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01176-2 · Cited by 41 · see citing works
Ramos-Prats, A., Paradiso, E., Castaldi, F., Sadeghi, M., Mir, M. Y., Hörtnagl, H., Göbel, G., & Ferraguti, F. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110893 · Cited by 37 · see citing works
Striatum-projecting prefrontal cortex neurons support working memory maintenance
Wilhelm, M., Sych, Y., Fomins, A., Warren, J. L. A., Lewis, C., Capdevila, L. S., Boehringer, R., Amadei, E. A., Grewe, B. F., O’Connor, E. C., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42777-3 · Cited by 39 · see citing works
“To achieve cellular resolution we used a wearable miniaturized microscope (miniscope) 41,42 and imaged mPFC neurons through a GRIN lens inserted into a chronically implanted cannula (Fig.”
MethodSpatial Representation of Hippocampal Place Cells in a T-Maze with an Aversive Stimulation
Okada, S., Igata, H., Sasaki, T., & Ikegaya, Y. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00101 · Cited by 37 · see citing works
“This finding is consistent with those observed in the other studies (Tronson et al., 2009; Grewe et al., 2017) and supports an idea that memory extinction is not a true elimination of learned aversive memory but is a formation of a new memory that aversive events are no longer present in the…”
ResultNeural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement
Aso, Y., Yamada, D., Bushey, D., Hibbard, K. L., Sammons, M., Otsuna, H., Shuai, Y., & Hige, T. (2023) · eLife · doi:10.7554/elife.85756 · Cited by 32 · see citing works
“As a neutral sensory stimulus (conditioned stimulus [CS]) is paired with punishment or reward (unconditioned stimulus [US]), the CS acquires the capacity to evoke valence-specific response patterns in the amygdala ( Grewe et al., 2017 ; Zhang and Li, 2018 ).”
BackgroundEngram mechanisms of memory linking and identity
Choucry, A., Nomoto, M., & Inokuchi, K. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00814-0 · Cited by 40 · see citing works
“One study showed that the CS-responding neuronal ensemble in the amygdala changed to resemble that of the US following successful association 43 , suggesting that there is crosstalk between sub-ensembles of the same memory.”
Memory engram stability and flexibility
Zaki, Y., & Cai, D. J. (2024) · Neuropsychopharmacology · doi:10.1038/s41386-024-01979-z · 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
Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala
Nguyen, R., Koukoutselos, K., Forro, T., & Ciocchi, S. (2023) · Science Advances · doi:10.1126/sciadv.adg4881 · Cited by 35 · see citing works
“During extinction learning, BLA glutamatergic inputs to the vH may convey an instructive signal of CS valence ( 70 ), inducing the formation of safety representations in the vH.”
BackgroundEffects of SSRI treatment on GABA and glutamate levels in an associative relearning paradigm
Spurny‐Dworak, B., Vanicek, T., Seiger, R., Reed, M. B., Klöbl, M., Ritter, V., Unterholzner, J., Godbersen, G. M., Silberbauer, L., Pacher, D., et al. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.117913 · Cited by 35 · see citing works
Brain Mechanisms Controlling Pavlovian Fear Conditioning
Yau, J., & McNally, G. (2018) · Journal of Experimental Psychology: Animal Learning and Cognition · doi:10.1037/xan0000181 · Cited by 23 · see citing works
- Authors
- Grewe, B. F., Gründemann, J., Kitch, L. J., Lecoq, J. A., Parker, J. G., Marshall, J. D., Larkin, M. C., Jercog, P. E., Grenier, F., Li, J. Z., Lüthi, A., & Schnitzer, M. J.
- Affiliations
- Howard Hughes Medical Institute (US)
- Friedrich Miescher Institute (CH)
- Pfizer (United States) (US)
- Stanford University (US)
- University of Basel (CH)
- Corresponding author
- Schnitzer, Mark J.
- ORCID
- Venue
- Nature
- Published
- 2017-03
- Volume
- 543
- Issue
- 7647
- Pages
- 670-675
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5378308
- OpenAlex
- W2602668040
- Cited by
- 351
- References
- 47
- Citations by year
- 2026: 27 · 2025: 31 · 2024: 44 · 2023: 45 · 2022: 27 · 2021: 34 · 2020: 42 · 2019: 46 · 2018: 36 · 2017: 19
- FWCI
- 22.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- 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 › Neural dynamics and brain function
- Keywords
- associative memory, neuronal ensembles, basal amygdala, lateral amygdala, fear conditioning, fear extinction, calcium dynamics, supervised learning, conditioned stimulus, unconditioned stimulus, microendoscopy
- MeSH terms
- Amygdala, Animals, Calcium, Conditioning, Classical, Extinction, Psychological, Fear, Male, Microscopy, Fluorescence, Neuronal Plasticity, Neurons, Calcium Signaling, Mice, Memory, Long-Term
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
