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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.
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“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
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BackgroundValue generalization in human avoidance learning
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“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 55
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
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
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
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 53
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
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
“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 51
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 55
Dunn, A. R., & Kaczorowski, C. C. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107069 · Cited by 42
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 56
“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 45
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 43
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
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 43
“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 42
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 44
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 43
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
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 39
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 45
“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
“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 35
“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 41
“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
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 44
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 36
“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 37
Brain mechanisms controlling Pavlovian fear conditioning.
Yau, J. O.-Y., & McNally, G. P. (2018) · Journal of Experimental Psychology Animal Learning and Cognition · doi:10.1037/xan0000181 · Cited by 35
Metadata
- 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
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