Goal-oriented searching mediated by ventral hippocampus early in trial-and-error learning
Abstract
Most behavioral learning in biology is trial and error, but how these learning processes are influenced by individual brain systems is poorly understood. Here we show that ventral-to-dorsal hippocampal subdivisions have specific and sequential functions in trial-and-error maze navigation, with ventral hippocampus (vH) mediating early task-specific goal-oriented searching. Although performance and strategy deployment progressed continuously at the population level, individual mice showed discrete learning phases, each characterized by particular search habits. Transitions in learning phases reflected feedforward inhibitory connectivity (FFI) growth occurring sequentially in ventral, then intermediate, then dorsal hippocampal subdivisions. FFI growth at vH occurred abruptly upon behavioral learning of goal-task relationships. vH lesions or the absence of vH FFI growth delayed early learning and disrupted performance consistency. Intermediate hippocampus lesions impaired intermediate place learning, whereas dorsal hippocampus lesions specifically disrupted late spatial learning. Trial-and-error navigational learning processes in naive mice thus involve a stereotype sequence of increasingly precise subtasks learned through distinct hippocampal subdivisions. Because of its unique connectivity, vH may relate specific goals to internal states in learning under healthy and pathological conditions.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
A recent mouse study has reported that units in ventral hippocampus mediate a form of goal-oriented search.
“In a similar vein, a recent mouse study has reported that units in ventral hippocampus, a region which is strongly connected to those supporting reward processing, mediates a form of goal-oriented search (Ruediger et al., 2012).”
From Goals and Habits in the Brain (2013) · cites this paper as Ruediger et al., 2012
Cites
Reinforcement Learning: An Introduction
Sutton, R. S., & Barto, A. G. (1998) · IEEE Transactions on Neural Networks · doi:10.1109/tnn.1998.712192 · Cited by 27,225 · see citing works
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
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 · see citing works
Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?
Fanselow, M. S., & Dong, H.-W. (2010) · Neuron · doi:10.1016/j.neuron.2009.11.031 · Cited by 3,358 · see citing works
Place Cells, Grid Cells, and the Brain's Spatial Representation System
Moser, E. I., Kropff, E., & Moser, M.-B. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.061307.090723 · Cited by 1,934 · see citing works
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697 · see citing works
The hippocampus and memory: insights from spatial processing
Bird, C. M., & Burgess, N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2335 · Cited by 1,313 · see citing works
Reduced fear expression after lesions of the ventral hippocampus
Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H.-A., Murison, R., Moser, E. I., & Moser, M.-B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152112399 · Cited by 912 · see citing works
Spatial learning with a minislab in the dorsal hippocampus.
Moser, M., Moser, E. I., Forrest, E., Andersen, P. N., & Morris, R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.21.9697 · Cited by 902 · see citing works
Reward, Motivation, and Reinforcement Learning
Dayan, P., & Balleine, B. W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00963-7 · Cited by 855 · see citing works
Hierarchically organized behavior and its neural foundations: A reinforcement learning perspective
Botvinick, M. M., Niv, Y., & Barto, A. G. (2009) · Cognition · doi:10.1016/j.cognition.2008.08.011 · Cited by 646 · see citing works
Adult-Generated Hippocampal Neurons Allow the Flexible Use of Spatially Precise Learning Strategies
Garthe, A., Behr, J., & Kempermann, G. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005464 · Cited by 597 · see citing works
Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories
Barnes, T. D., Kubota, Y., Hu, D., Jin, D. Z., & Graybiel, A. M. (2005) · Nature · doi:10.1038/nature04053 · Cited by 595 · see citing works
The learning curve: implications of a quantitative analysis.
Gallistel, C., Fairhurst, S. P., & Balsam, P. (2004) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0404965101 · Cited by 587 · see citing works
Distinct components of spatial learning revealed by prior training and NMDA receptor blockade
Bannerman, D. M., Good, M. A., Butcher, S. P., Ramsay, M., & Morris, R. G. M. (1995) · Nature · doi:10.1038/378182a0 · Cited by 551 · see citing works
Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area
Luo, A. H., Tahsili-Fahadan, P., Wise, R. A., Lupica, C. R., & Aston-Jones, G. (2011) · Science · doi:10.1126/science.1204622 · Cited by 425 · see citing works
Thorn, C. A., Atallah, H. E., Howe, M. W., & Graybiel, A. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.036 · Cited by 412 · see citing works
Genomic anatomy of the hippocampus
Thompson, C. L., Pathak, S. D., Jeromin, A., Ng, L. L., MacPherson, C. R., Mortrud, M. T., Cusick, A., Riley, Z. L., Sunkin, S. M., Bernard, A., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.12.008 · Cited by 403 · see citing works
Genomic–anatomic evidence for distinct functional domains in hippocampal field CA1
Dong, H., Swanson, L. W., Chen, L., Fanselow, M. S., & Toga, A. W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812608106 · Cited by 361 · see citing works
Distinct Representations and Theta Dynamics in Dorsal and Ventral Hippocampus
Royer, S., Sirota, A., Patel, J., & Buzsáki, G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4681-09.2010 · Cited by 351 · see citing works
The Hippocampus Plays a Selective Role in the Retrieval of Detailed Contextual Memories
Wiltgen, B. J., Zhou, M., Cai, Y., Balaji, J., Karlsson, M. G., Parivash, S. N., Li, W., & Silva, A. J. (2010) · Current Biology · doi:10.1016/j.cub.2010.06.068 · Cited by 300 · see citing works
The hippocampal-striatal axis in learning, prediction and goal-directed behavior
Pennartz, C. M. A., Ito, R., Verschure, P. F. M. J., Battaglia, F. P., & Robbins, T. W. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.08.001 · Cited by 287 · see citing works
Learning-related feedforward inhibitory connectivity growth required for memory precision
Ruediger, S., Vittori, C. G., Bednarek, E., Genoud, C., Strata, P., Sacchetti, B., & Caroni, P. (2011) · Nature · doi:10.1038/nature09946 · Cited by 282 · see citing works
Self-citationBethus, I., Tse, D., & Morris, R. G. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2721-09.2010 · Cited by 270 · see citing works
AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks
Paola, V. D., Arber, S., & Caroni, P. (2003) · Nature Neuroscience · doi:10.1038/nn1046 · Cited by 236 · see citing works
Self-citationSearch Strategies Used byAPPTransgenic Mice During Navigation in the Morris Water MazePreprint
Janus, C. (2004) · Learning & Memory · doi:10.1101/lm.70104 · Cited by 194 · see citing works
From Rapid Place Learning to Behavioral Performance: A Key Role for the Intermediate Hippocampus
Bast, T., Wilson, I. A., Witter, M. P., & Morris, R. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000089 · Cited by 189 · see citing works
Wolfer, D. P., & Lipp, H. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.02095.x · Cited by 165 · see citing works
Bednarek, E., & Caroni, P. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.034 · Cited by 160 · see citing works
Self-citationAnterior hippocampus and goal-directed spatial decision making
Viard, A., Doeller, C. F., Hartley, T., Bird, C. M., & Burgess, N. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4640-10.2011 · Cited by 144 · see citing works
Dynamic Coding of Goal-Directed Paths by Orbital Prefrontal Cortex
Young, J., & Shapiro, M. L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5436-10.2011 · Cited by 81 · see citing works
Impaired Synaptic Plasticity and Learning in Mice Lacking β-Adducin, an Actin-Regulating Protein
Rabenstein, R. L., Addy, N., Caldarone, B. J., Asaka, Y., Gruenbaum, L. M., Peters, L. L., Gilligan, D. M., Fitzsimonds, R. M., & Picciotto, M. R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3530-04.2005 · Cited by 76 · see citing works
Amemori, K., Gibb, L., & Graybiel, A. M. (2011) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2011.00047 · Cited by 72 · see citing works
Hoh, T., Beiko, J., Boon, F. H., Weiss, S., & Cain, D. P. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-10-j0003.1999 · Cited by 65 · see citing works
Optimal habits can develop spontaneously through sensitivity to local cost
Desrochers, T. M., Jin, D. Z., Goodman, N. D., & Graybiel, A. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013470107 · Cited by 43 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Dolan, R. J., & Dayan, P. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.007 · Cited by 977 · see citing works
Hippocampal–prefrontal input supports spatial encoding in working memory
Spellman, T., Rigotti, M., Ahmari, S. E., Fusi, S., Gogos, J. A., & Gordon, J. A. (2015) · Nature · doi:10.1038/nature14445 · Cited by 693 · see citing works
Evensmoen, H. R., Ladstein, J., Hansen, T. I., Møller, J. A., Witter, M. P., Nadel, L., & Håberg, A. K. (2015) · Hippocampus · doi:10.1002/hipo.22357 · Cited by 75 · see citing works
- Authors
- Ruediger, S., Spirig, D., Donato, F., & Caroni, P.
- Affiliations
- Friedrich Miescher Institute (CH)
- Corresponding author
- Caroni, Pico
- Venue
- Nature Neuroscience
- Published
- 2012-09-23
- Volume
- 15
- Issue
- 11
- Pages
- 1563-1571
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2045981980
- Cited by
- 135
- References
- 37
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 8 · 2023: 10 · 2022: 11 · 2021: 12 · 2020: 12 · 2019: 7 · 2018: 8 · 2017: 10 · 2016: 12 · 2015: 16 · 2014: 9 · 2013: 4
- FWCI
- 4.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- edoc (University of Basel) (submittedVersion)
- Funders
- École Polytechnique Fédérale de Lausanne
- 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, trial-and-error learning, dorsal hippocampus, spatial learning, place learning, learning stages, search strategies
- MeSH terms
- Adducins, Animals, Benzazepines, Brain Mapping, Conditioning, Psychological, Cytoskeletal Proteins, Exploratory Behavior, Fear, Goals, Hippocampus, Learning, Male, Mice, Transgenic, Microfilament Proteins, Neural Inhibition, Neurons, Phosphopyruvate Hydratase, Time Factors, Proto-Oncogene Proteins c-fos, Dopamine Antagonists, Maze Learning, Green Fluorescent Proteins, Mice
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
