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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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InfluentialAcute Food Deprivation Rapidly Modifies Valence-Coding Microcircuits in the AmygdalaPreprint
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Hippocampus as a sorter and reverberatory integrator of sensory inputs
Nomoto, M., Murayama, E., Ohno, S., Okubo-Suzuki, R., Muramatsu, S., & Inokuchi, K. (2022) · Nature Communications · doi:10.1038/s41467-022-35119-2 · Cited by 16
Webler, R. D., Oathes, D. J., van Rooij, S. J. H., Gewirtz, J. C., Nahas, Z. H., Lissek, S. M., & Widge, A. S. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.105005 · Cited by 14
Veres, J. M., Fekete, Z., Müller, K., Andrási, T., Rovira-Esteban, L., Barabás, B., Papp, O. I., & Hájos, N. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1120338 · Cited by 14
“, 2017), a portion of which is engaged in memory processes or pain processing does not exceed typically 10–15% (Trouche et al., 2013; Senn et al., 2014; Grewe et al., 2017; Corder et al., 2019).”
All IEGs Are Not Created Equal—Molecular Sorting Within the Memory Engram
Yelhekar, T. D., Meng, M., Doupe, J., & Lin, Y. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-62983-9_6 · Cited by 12
Investigating learning-related neural circuitry with chronic in vivo optical imaging
Lee, C. R., Najafizadeh, L., & Margolis, D. J. (2020) · Brain Structure and Function · doi:10.1007/s00429-019-02001-9 · Cited by 12
Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning
Asokan, M. M., Watanabe, Y. L., Kimchi, E. Y., & Polley, D. B. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113167 · Cited by 15
Prefrontal circuits encode both general danger and specific threat representations
Martín‐Fernández, M., Menegolla, A. P., Lopez-Fernandez, G., Winke, N., Jercog, D., Kim, H.-R., Girard, D., Déjean, C., & Herry, C. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01472-8 · Cited by 16
“In the amygdala, the CS + neuronal representation becomes more similar to the US neuronal representation after conditioning 18 .”
MethodPoggi, G., Bergamini, G., Dulinskas, R., Madur, L., Greter, A., Ineichen, C., Dagostino, A., Kúkeľová, D., Sigrist, H., Bornemann, K. D., et al. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16272 · Cited by 12
“10 12 vg/mL, 300 nL) (Grewe et al., 2017; Madur et al., 2023), was injected unilaterally in the BA (see Stereotactic surgery for retrograde tracing and fibre photometry).”
MethodExtracellular matrix: a new player in memory maintenance and psychiatric disorders
Bach, D. R., Brown, S. A., Kleim, B., & Tyagarajan, S. K. (2019) · Swiss Medical Weekly · doi:10.4414/smw.2019.20060 · Cited by 11
Ca2+ imaging of neurons in freely moving rats with automatic post hoc histological identification
Anner, P., Passecker, J., Klausberger, T., & Dorffner, G. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.108765 · Cited by 12
Imaging distinct neuronal populations with a dual channel miniscope
Barbera, G., Thapa, R., Adhikari, N., Li, Y., & Lin, D. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1445020 · Cited by 11
Synaptic dysfunction in amygdala in intellectual disorder models
Aincy, M., Méziane, H., Hérault, Y., & Humeau, Y. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.07.028 · Cited by 11
Andreani, J. C. (2021) · NeuroTarget · doi:10.47924/neurotarget20213 · Cited by 10
Lateral ventral tegmental area GABAergic and glutamatergic modulation of conditioned learning
Rizzi, G., Li, Z., Hogrefe, N., & Tan, K. R. (2020) · Cell Reports · doi:10.1016/j.celrep.2021.108867 · Cited by 10
Svalina, M. N., Guthman, E. M., Rio, C. A. C.-D., Kushner, J. K., Baca, S. M., Restrepo, D., & Huntsman, M. M. (2021) · eNeuro · doi:10.1523/eneuro.0113-21.2021 · Cited by 12
Magnetic voluntary head-fixation in transgenic rats enables lifespan imaging of hippocampal neurons
Rich, P. D., Thiberge, S. Y., Scott, B. B., Guo, C., Tervo, D. G. R., Brody, C. D., Karpova, A. Y., Daw, N. D., & Tank, D. W. (2024) · Nature Communications · doi:10.1038/s41467-024-48505-9 · Cited by 10
“Single photon imaging has been used to track cells over multiple days 45,53 but is challenging over longer periods due to lack of optical sectioning, light scattering and its ability to only visualize active cells 54 .”
Stability of cross-sensory input to primary somatosensory cortex across experience
Kato, D. D., & Bruno, R. M. (2024) · Neuron · doi:10.1016/j.neuron.2024.10.020 · Cited by 10
“77 By contrast, passively pairing an auditory and visual stimulus does specifically increase V1 responses to the paired auditory stimulus.”
Contributions of associative and non-associative learning to the dynamics of defensive ethograms
Le, Q.-S. E., Hereford, D., Borkar, C. D., Aldaco, Z., Klar, J., Resendez, A., & Fadok, J. P. (2024) · eLife · doi:10.7554/elife.90414.3 · Cited by 9
Npas4-mediated dopaminergic regulation of safety memory consolidation
Ko, B., Yoo, J.-Y., Yoo, T., Choi, W., Dogan, R., Sung, K., Um, D., Lee, S. B., Kim, H. J., Lee, S., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112678 · Cited by 9
Turning strains into strengths for understanding psychiatric disorders
Moore, S. J., Murphy, G. G., & Cazares, V. A. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0772-y · Cited by 10
“, in genes, sex, and environment) alter neurophysiological mechanisms that lead to susceptibility or resiliency (for example, by visualizing neural circuit activity during FE learning [69]).”
BackgroundWhat is a cognitive map? Organising knowledge for flexible behaviourPreprint
Behrens, T. E. J., Müller, T., Whittington, J. C. R., Mark, S., Baram, A. B., Stachenfeld, K., & Kurth-Nelson, Z. L. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/365593 · Cited by 16
“Indeed, such mechanisms likely do exist in the brain (e.g. in (Grewe et al., 2017)).”
BackgroundLink Brain-Wide Projectome to Neuronal Dynamics in the Mouse Brain
Li, X., Du, Y., Huang, J., Li, W.-W., Song, W., Fan, R.-N., Zhou, H. K., Jiang, T., Lu, C., Guan, Z., et al. (2024) · Neuroscience Bulletin · doi:10.1007/s12264-024-01232-z · Cited by 8
Salient safety conditioning improves novel discrimination learning
Nahmoud, I., Vasquez, J. G., Cho, H., Dennis‐Tiwary, T. A., & Likhtik, E. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112907 · Cited by 10
More, J., Casas, M. M., Sánchez, G., Hidalgo, C., & Haeger, P. A. (2018) · Neural Plasticity · doi:10.1155/2018/5056181 · Cited by 8
“Fear conditioning, an associative learning process that produces robust memories, represents a form of Pavlovian conditioning that has received considerable attention over the last years [1, 2].”
A behavioral perspective on service center routing: The role of inertia
Schecter, A., Wowak, K. D., Berente, N., Ye, H., & Mukherjee, U. K. (2021) · Journal of Operations Management · doi:10.1002/joom.1156 · Cited by 8
Excitability-Independent Memory Allocation for Repeated Event
Cho, H.-Y., Lee, H.-S., Jeong, Y., Han, J., Yoo, M., & Han, J. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.860027 · Cited by 8
“Liu et al., 2012; Josselyn et al., 2015; Tonegawa et al., 2015; Grewe et al., 2017).”
Robinson, K. J., Everett, N. A., Baracz, S. J., & Cornish, J. L. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06175-9 · Cited by 8
A Marr's Three‐Level Analytical Framework for Neuromorphic Electronic Systems
Guo, Y., Zou, X., Hu, Y., Yang, Y., Wang, X., He, Y., Kong, R., Guo, Y., Li, G., Zhang, W., et al. (2021) · Advanced Intelligent Systems · doi:10.1002/aisy.202100054 · Cited by 14
The hippocampus contributes to retroactive stimulus associations during trace fear conditioning
Puhger, K. R., Crestani, A. P., Diniz, C. R. A. F., & Wiltgen, B. J. (2024) · iScience · doi:10.1016/j.isci.2024.109035 · Cited by 9
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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