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A Role for the Locus Coeruleus in Hippocampal CA1 Place Cell Reorganization during Spatial Reward Learning
Open accessAbstract
During spatial learning, hippocampal (HPC) place maps reorganize to represent new goal locations, but little is known about the circuit mechanisms facilitating these changes. Here, we examined how neuromodulation via locus coeruleus (LC) projections to HPC area CA1 (LC-CA1) regulates the overrepresentation of CA1 place cells near rewarded locations. Using two-photon calcium imaging, we monitored the activity of LC-CA1 fibers in the mouse dorsal HPC. We find that the LC-CA1 projection signals the translocation of a reward, predicting behavioral performance on a goal-oriented spatial learning task. An optogenetic stimulation mimicking this LC-CA1 activity induces place cell reorganization around a familiar reward, while its inhibition decreases the degree of overrepresentation around a translocated reward. Our results show that LC acts in conjunction with other factors to induce goal-directed reorganization of HPC representations and provide a better understanding of the role of neuromodulatory actions on HPC place map plasticity.
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“Notably, stimulation of locus coeruleus neurons, presumably releasing noradrenaline or dopamine, enhances hippocampus-dependent memory [105–108].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [108]
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Cites
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010
Cognitive maps in rats and men
Tolman, E. C. (1948) · Psychological Review · doi:10.1037/h0061626 · Cited by 6,641
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151
The hippocampus as a cognitive map
Passingham, R. E. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90015-0 · Cited by 5,128
Nucleus locus ceruleus: new evidence of anatomical and physiological specificity
Foote, S. L., Bloom, F. E., & Aston-Jones, G. (1983) · Physiological Reviews · doi:10.1152/physrev.1983.63.3.844 · Cited by 1,901
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
Orienting and reorienting: the locus coeruleus mediates cognition through arousal
Sara, S. J., & Bouret, S. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.011 · Cited by 1,056
The hippocampus as a predictive map
Stachenfeld, K. L., Botvinick, M. M., & Gershman, S. J. (2017) · Nature Neuroscience · doi:10.1038/nn.4650 · Cited by 1,000
Astrocyte calcium signaling: the third wave
Bazargani, N., & Attwell, D. (2016) · Nature Neuroscience · doi:10.1038/nn.4201 · Cited by 999
Functional imaging of hippocampal place cells at cellular resolution during virtual navigation
Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L., & Tank, D. W. (2010) · Nature Neuroscience · doi:10.1038/nn.2648 · Cited by 873
Locus coeruleus and dopaminergic consolidation of everyday memory
Takeuchi, T., Duszkiewicz, A. J., Sonneborn, A., Spooner, P. A., Yamasaki, M., Watanabe, M., Smith, C. C., Fernández, G., Deisseroth, K., Greene, R. W., et al. (2016) · Nature · doi:10.1038/nature19325 · Cited by 827
The reorganization and reactivation of hippocampal maps predict spatial memory performance
Dupret, D., O'Neill, J., Pleydell-Bouverie, B., & Csicsvari, J. (2010) · Nature Neuroscience · doi:10.1038/nn.2599 · Cited by 769
Behavioral time scale synaptic plasticity underlies CA1 place fields
Bittner, K. C., Milstein, A. D., Grienberger, C., Romani, S., & Magee, J. C. (2017) · Science · doi:10.1126/science.aan3846 · Cited by 707
Kempadoo, K. A., Mosharov, E. V., Choi, S. J., Sulzer, D., & Kandel, E. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616515114 · Cited by 647
Rapid signalling in distinct dopaminergic axons during locomotion and reward
Howe, M. W., & Dombeck, D. A. (2016) · Nature · doi:10.1038/nature18942 · Cited by 618
Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons
Bittner, K. C., Grienberger, C., Vaidya, S. P., Milstein, A. D., Macklin, J. J., Suh, J., Tonegawa, S., & Magee, J. C. (2015) · Nature Neuroscience · doi:10.1038/nn.4062 · Cited by 540
Increased Attention to Spatial Context Increases Both Place Field Stability and Spatial Memory
Kentros, C. G., Agnihotri, N. T., Streater, S., Hawkins, R. D., & Kandel, E. R. (2004) · Neuron · doi:10.1016/s0896-6273(04)00192-8 · Cited by 537
An Information-Theoretic Approach to Deciphering the Hippocampal Code
Skaggs, W. E., McNaughton, B. L., & Gothard, K. M. (1992) · Cited by 511
Dendritic Inhibition in the Hippocampus Supports Fear Learning
Lovett-Barron, M., Kaifosh, P., Kheirbek, M. A., Danielson, N., Zaremba, J. D., Reardon, T. R., Turi, G. F., Hen, R., Zemelman, B. V., & Losonczy, A. (2014) · Science · doi:10.1126/science.1247485 · Cited by 509
Self-citationProjections from neocortex mediate top-down control of memory retrieval
Rajasethupathy, P., Sankaran, S., Marshel, J. H., Kim, C. K., Ferenczi, E., Lee, S. Y., Berndt, A., Ramakrishnan, C., Jaffe, A., Lo, M., et al. (2015) · Nature · doi:10.1038/nature15389 · Cited by 509
Accumulation of Hippocampal Place Fields at the Goal Location in an Annular Watermaze Task
Hollup, S., Molden, S., Donnett, J. G., Moser, M., & Moser, E. I. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01635.2001 · Cited by 491
Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence
McNamara, C. G., Tejero-Cantero, Á., Trouche, S., Campo-Urriza, N., & Dupret, D. (2014) · Nature Neuroscience · doi:10.1038/nn.3843 · Cited by 486
Understanding memory through hippocampal remapping
Colgin, L. L., Moser, E. I., & Moser, M.-B. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.06.008 · Cited by 450
Central Cholinergic Neurons Are Rapidly Recruited by Reinforcement Feedback
Hangya, B., Ranade, S. P., Lorenc, M., & Kepecs, A. (2015) · Cell · doi:10.1016/j.cell.2015.07.057 · Cited by 399
A Dedicated Population for Reward Coding in the Hippocampus
Gauthier, J. L., & Tank, D. W. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.008 · Cited by 394
Parallel emergence of stable and dynamic memory engrams in the hippocampus
Hainmueller, T., & Bartos, M. (2018) · Nature · doi:10.1038/s41586-018-0191-2 · Cited by 392
Active control of arousal by a locus coeruleus GABAergic circuit
Breton‐Provencher, V., & Sur, M. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0305-z · Cited by 377
Bouret, S., & Sara, S. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03526.x · Cited by 371
Global Representations of Goal-Directed Behavior in Distinct Cell Types of Mouse Neocortex
Allen, W. E., Kauvar, I., Chen, M. Z., Richman, E. B., Yang, S., Chan, K. Y., Gradinaru, V., Deverman, B. E., Luo, L., & Deisseroth, K. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.017 · Cited by 366
Novelty and Dopaminergic Modulation of Memory Persistence: A Tale of Two Systems
Duszkiewicz, A. J., McNamara, C. G., Takeuchi, T., & Genzel, L. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.10.002 · Cited by 324
Cell-Type-Specific Activity in Prefrontal Cortex during Goal-Directed Behavior
Pinto, L., & Dan, Y. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.021 · Cited by 323
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
Self-citationLocus coeruleus input to hippocampal CA3 drives single-trial learning of a novel context
Wagatsuma, A., Okuyama, T., Sun, C., Smith, L. M., Abe, K., & Tonegawa, S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714082115 · Cited by 283
Locus coeruleus: From global projection system to adaptive regulation of behavior
Aston‐Jones, G., & Waterhouse, B. D. (2016) · Brain Research · doi:10.1016/j.brainres.2016.03.001 · Cited by 268
Hippocampal place cells: stereotypy and plasticity
Breese, C., Hampson, R., & Deadwyler, S. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-04-01097.1989 · Cited by 255
Goal-Related Activity in Hippocampal Place Cells
Hok, V., Lenck‐Santini, P., Roux, S., Save, É., Muller, R. U., & Poucet, B. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2864-06.2007 · Cited by 245
Coordinated forms of noradrenergic plasticity in the locus coeruleus and primary auditory cortex
Martins, A. R. O., & Froemke, R. C. (2015) · Nature Neuroscience · doi:10.1038/nn.4090 · Cited by 233
SIMA: Python software for analysis of dynamic fluorescence imaging data
Kaifosh, P., Zaremba, J. D., Danielson, N., & Losonczy, A. (2014) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2014.00080 · Cited by 220
Self-citationTuri, G. F., Li, W.-K., Chavlis, S., Pandi, I., O’Hare, J., Priestley, J. B., Grosmark, A. D., Liao, Z., Ladow, M., Zhang, J. F., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.009 · Cited by 218
Self-citationTransgenic expression of Cre recombinase from the tyrosine hydroxylase locus
Lindeberg, J., Usoskin, D., Bengtsson, H., Gustafsson, A., Kylberg, A., Söderström, S., & Ebendal, T. (2004) · genesis · doi:10.1002/gene.20065 · Cited by 211
Hippocampal Neurons Responding to First-Time Dislocation of a Target Object
Fyhn, M., Molden, S., Hollup, S., Moser, M., & Moser, E. I. (2002) · Neuron · doi:10.1016/s0896-6273(02)00784-5 · Cited by 202
In vivo two-photon imaging of sensory-evoked dendritic calcium signals in cortical neurons
Jia, H., Rochefort, N. L., Chen, X., & Konnerth, A. (2010) · Nature Protocols · doi:10.1038/nprot.2010.169 · Cited by 196
VTA neurons coordinate with the hippocampal reactivation of spatial experience
Gomperts, S. N., Kloosterman, F., & Wilson, M. A. (2015) · eLife · doi:10.7554/elife.05360 · Cited by 191
Neuromodulation of hippocampal long-term synaptic plasticity
Palacios-Filardo, J., & Mellor, J. R. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.08.009 · Cited by 184
CNS Dopamine Transmission Mediated by Noradrenergic Innervation
Smith, C. C., & Greene, R. W. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6486-11.2012 · Cited by 177
Task-Dependent Representations in Rat Hippocampal Place Neurons
Kobayashi, T., Nishijo, H., Fukuda, M., Bureš, J., & Ono, T. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.2.597 · Cited by 155
Hippocampal 5-HT Input Regulates Memory Formation and Schaffer Collateral Excitation
Teixeira, C. M., Rosen, Z. B., Suri, D., Sun, Q., Hersh, M. A., Sargin, D., Dincheva, I., Morgan, A. A., Spivack, S., Krok, A. C., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.04.030 · Cited by 140
Impaired hippocampal place cell dynamics in a mouse model of the 22q11.2 deletion
Zaremba, J. D., Diamantopoulou, A., Danielson, N., Grosmark, A., Kaifosh, P., Bowler, J. C., Liao, Z., Sparks, F. T., Gogos, J. A., & Losonczy, A. (2017) · Nature Neuroscience · doi:10.1038/nn.4634 · Cited by 126
Self-citationXu, H., Baracskay, P., O’Neill, J., & Csicsvari, J. (2018) · Neuron · doi:10.1016/j.neuron.2018.11.015 · Cited by 109
Locus coeruleus activation accelerates perceptual learning
Glennon, E., Carcea, I., Martins, A. R. O., Multani, J., Shehu, I., Svirsky, M. A., & Froemke, R. C. (2018) · Brain Research · doi:10.1016/j.brainres.2018.05.048 · Cited by 92
Coordination of rapid cholinergic and dopaminergic signaling in striatum during spontaneous movement
Howe, M. W., Ridouh, I., Mascaro, A. L. A., Larios, A., Azcorra, M., & Dombeck, D. A. (2019) · eLife · doi:10.7554/elife.44903 · Cited by 84
The Michelin red guide of the brain: role of dopamine in goal-oriented navigation
Retailleau, A., & Boraud, T. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00032 · Cited by 42
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Poe, G. R., Foote, S., Eschenko, O., Johansen, J. P., Bouret, S., Aston-Jones, G., Harley, C. W., Manahan-Vaughan, D., Weinshenker, D., Valentino, R., et al. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0360-9 · Cited by 720
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Self-citation
Metadata
- Authors
- Kaufman, A. M., Geiller, T., & Losonczy, A.
- Affiliations
- Mortimer B. Zuckerman Mind Brain Behavior Institute (US)
- Corresponding author
- Losonczy, Attila
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2020-03
- Volume
- 105
- Issue
- 6
- Pages
- 1018-1026.e4
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC7265133
- OpenAlex
- W3002023792
- Cited by
- 193
- References
- 53
- Citations by year
- 2026: 31 · 2025: 34 · 2024: 41 · 2023: 27 · 2022: 25 · 2021: 23 · 2020: 11
- FWCI
- 11.48
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 382 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Foundation for the National Institutes of Health
- Kavli Foundation
- National Science Foundation (DGE-1644869, 1F31MH117870-01A1)
- 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
- locus coeruleus, hippocampal CA1, place cells, neuromodulation, goal-directed learning, optogenetic stimulation
- MeSH terms
- Place Cells, Animals, Female, Locus Coeruleus, Male, Mice, Transgenic, Neural Inhibition, Neural Pathways, Reward, Mice, CA1 Region, Hippocampal, Optogenetics, Spatial Learning
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