Cited by 218Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

The DOI matches its Crossref record; 82 of the 82 references it cites were found in a registry or an index.

Vasoactive Intestinal Polypeptide-Expressing Interneurons in the Hippocampus Support Goal-Oriented Spatial Learning

Open access

Turi, Gergely Farkas, Li, Wen-Ke, Chavlis, Spyridon, Pandi, Ioanna, O’Hare, Justin, Priestley, James Benjamin, Grosmark, Andres Daniel, Liao, Zhenrui, Ladow, Max, Zhang, Jeff Fang, Zemelman, Boris Valery, Poirazi, Panayiota, Losonczy, Attila·2019·Neuron

DOI 10.1016/j.neuron.2019.01.009PMC PMC6428605

Open this paper in CoChat — free account Open PDF

Abstract

Diverse computations in the neocortex are aided by specialized GABAergic interneurons (INs), which selectively target other INs. However, much less is known about how these canonical disinhibitory circuit motifs contribute to network operations supporting spatial navigation and learning in the hippocampus. Using chronic two-photon calcium imaging in mice performing random foraging or goal-oriented learning tasks, we found that vasoactive intestinal polypeptide-expressing (VIP+), disinhibitory INs in hippocampal area CA1 form functional subpopulations defined by their modulation by behavioral states and task demands. Optogenetic manipulations of VIP+ INs and computational modeling further showed that VIP+ disinhibition is necessary for goal-directed learning and related reorganization of hippocampal pyramidal cell population dynamics. Our results demonstrate that disinhibitory circuits in the hippocampus play an active role in supporting spatial learning. VIDEO ABSTRACT.

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

Crossref · 10.1016/j.neuron.2019.01.009

Cites

82 of 82 references verified0 citation errors · 0 not checkable

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Scikit-learn: Machine Learning in Python
Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Müller, A., Nothman, J., Louppe, G., et al. (2012) · arXiv · doi:10.48550/arxiv.1201.0490 · Cited by 71,016
The mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859
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
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,478
The NEURON Simulation Environment
Hines, M. L., & Carnevale, N. T. (1997) · Neural Computation · doi:10.1162/neco.1997.9.6.1179 · Cited by 2,630
Dynamics of the Hippocampal Ensemble Code for Space
Wilson, M. A., & McNaughton, B. L. (1993) · Science · doi:10.1126/science.8351520 · Cited by 2,350
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050
A cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,815
Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons
Pfeffer, C. K., Xue, M., He, M., Huang, Z. J., & Scanziani, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3446 · Cited by 1,353

Flagged first, then by citations

Show all 82 references

Sorted by citations

Items 101–200 of 218

Goal-specific hippocampal inhibition gates learning
Jeong, N., Zheng, X. X., Paulson, A. L., Prince, S., Nguyen, V. P., Thomas, S. R., Gilpin, C. E., Goodson, M. C., & Singer, A. C. (2025) · Nature · doi:10.1038/s41586-025-08868-5 · Cited by 14
31st Annual Computational Neuroscience Meeting: CNS*2022
Corsi, M., Sorrentino, P., Schwartz, D., George, N., Hugueville, L., Kahn, A. E., Dupont, S., Bassett, D. S., Jirsa, V., & Fallani, F. D. V. (2023) · Journal of Computational Neuroscience · doi:10.1007/s10827-022-00841-9 · Cited by 11
Rapid neocortical network modifications via dendritic plateau potential induced plasticityPreprint
Xiao, K., Li, Y., Sullivan, B. J., Li, G., & Magee, J. C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.19.689338 · Cited by 18
Computationally going where experiments cannot: a dynamical assessment of dendritic ion channel currents during in vivo-like states
Guet-McCreight, A., & Skinner, F. K. (2020) · F1000Research · doi:10.12688/f1000research.22584.2 · Cited by 14
Multiphoton imaging of hippocampal neural circuits: techniques and biological insights into region-, cell-type-, and pathway-specific functions
Mizuta, K., & Sato, M. (2024) · Neurophotonics · doi:10.1117/1.nph.11.3.033406 · Cited by 8
A Characterization of the Electrophysiological and Morphological Properties of Vasoactive Intestinal Peptide (VIP) Interneurons in the Medial Entorhinal Cortex (MEC)
Badrinarayanan, S., Manseau, F., Lim, B. K., Williams, S., & Brandon, M. P. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.653116 · Cited by 8
Breakdown of spatial coding and neural synchronization in epilepsyPreprint
Shuman, T., Aharoni, D. B., Cai, D. J., Lee, C. R., Chavlis, S., Taxidis, J., Flores, S. E., Cheng, K., Javaherian, M., Kaba, C. C., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/358580 · Cited by 9
Self-citation
Neuro-Inspired Reinforcement Learning to Improve Trajectory Prediction in Reward-Guided Behavior
Chen, B., Yang, S., Kuo, C., Chen, J., Lo, Y., Kuo, Y.-T., Lin, Y.-C., Chang, H.-C., Lin, S.-H., Yu, X., et al. (2022) · International Journal of Neural Systems · doi:10.1142/s0129065722500381 · Cited by 9
The role of astrocytes in place cell formation: A computational modeling study
Polykretis, I., & Michmizos, K. P. (2022) · Journal of Computational Neuroscience · doi:10.1007/s10827-022-00828-6 · Cited by 5
An Intranet of Things approach for adaptable control of behavioral and navigation-based experiments
Bowler, J. C., Zakka, G., Yong, H. C., Li, W., Rao, B. Y., Liao, Z., Priestley, J. B., & Losonczy, A. (2024) · eLife · doi:10.7554/elife.97433 · Cited by 5
Self-citation
Behavioral timescale synaptic plasticity: properties, elements and functions
Magee, J. C. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02214-2 · Cited by 10
All-optical electrophysiology reveals behavior-dependent dynamics of excitation and inhibition in the hippocampus
Yang, Q., Baror-Sebban, S., Kipper, R., London, M., & Adam, Y. (2026) · Neuron · doi:10.1016/j.neuron.2025.12.040 · Cited by 12
Conditioning and pseudoconditioning differently change intrinsic excitability of inhibitory interneurons in the neocortex
Kanigowski, D., & Urban‐Ciećko, J. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhae109 · Cited by 6
Learning-dependent feedback by OLM interneurons shapes CA1 representationsPreprint
Campbell, E. P., Martin, L., Magee, J. C., & Grienberger, C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.21.695825 · Cited by 11
mTORC1-mediated acquisition of reward-related representations by hippocampal somatostatin interneurons
Michon, F.-X., Laplante, I., Bosson, A., Robitaille, R., & Lacaille, J. (2023) · Molecular Brain · doi:10.1186/s13041-023-01042-w · Cited by 7
Morpho‐physiological properties and connectivity of vasoactive intestinal polypeptide‐expressing interneurons in the mouse hippocampal dentate gyrus
Yuting, W., Wu, J., Yeh, C., Shen, H., Wu, K., Vida, I., & Lien, C. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25116 · Cited by 5
Distinct brain-wide presynaptic networks underlie the functional identity of individual cortical neuronsPreprint
Inácio, A. R. L., Lam, K. C., Zhao, Y., Pereira, F., Gerfen, C. R., & Lee, S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.25.542329 · Cited by 6
Impact of Dendritic Spine Loss on Excitability of Hippocampal CA1 Pyramidal Neurons: A Computational Study of Early Alzheimer Disease
Tian, C., Reyes, I., Johnson, A., & Masurkar, A. V. (2025) · Hippocampus · doi:10.1002/hipo.70025 · Cited by 6
Differential vulnerability of anterior cingulate cortex cell types to diseases and drugs
Smail, M. A., Chandrasena, S. S., Zhang, X., Reddy, V., Kelley, C., Herman, J. P., Sherif, M., McCullumsmith, R. E., & Shukla, R. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01657-w · Cited by 5
Serotonin modulates infraslow oscillation in the dentate gyrus during non-REM sleep
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2024) · eLife · doi:10.7554/elife.100196.4 · Cited by 24
Self-citation
Synaptogenic activity of the axon guidance molecule Robo2 is critical for hippocampal circuit functionPreprint
Blockus, H., Rolotti, S. V., Szoboszlay, M., Ming, T., Schroeder, A., Vennekens, K. M., Katsamba, P. S., Bahna, F. A., Mannepalli, S. M., Ahlsén, G., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/840710 · Cited by 5
Self-citation
Medial entorhinal cortex plays a specialized role in learning of flexible, context-dependent interval timing behaviorPreprint
Bigus, E. R., Lee, H., Bowler, J. C., Shi, J., & Heys, J. G. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.18.524598 · Cited by 5
Synaptic Plasticity in the Hippocampus
Bliss, T., Collingridge, G. L., Cooke, S. F., Georgiou, J., & Morris, R. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0010 · Cited by 4
Brain region-specific gain modulation of place cells by VIP neurons
Lenkey, N., Garvert, A. C., Neubrandt, M., Kriener, B., & Vervaeke, K. (2025) · Nature Communications · doi:10.1038/s41467-025-60679-4 · Cited by 5
Deciphering how interneuron specific 3 cells control oriens lacunosum-moleculare cells to contribute to circuit function
Guet-McCreight, A., & Skinner, F. K. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00204.2021 · Cited by 4
Predictive goal coding by dentate gyrus somatostatin-expressing interneurons in male mice
Yuan, M., Cazala, A., Goedeke, S., Leibold, C., Sauer, J., & Bartos, M. (2025) · Nature Communications · doi:10.1038/s41467-025-60841-y · Cited by 4
Hippocampal place code plasticity in CA1 requires postsynaptic membrane fusion
Plitt, M. H., Kaganovsky, K., Say, E., Sosa, M., Südhof, T. C., & Giocomo, L. M. (2026) · Neuron · doi:10.1016/j.neuron.2026.03.006 · Cited by 7
Rare mutations implicate CGE interneurons as a vulnerable axis of cognitive deficits across psychiatric disordersPreprint
Herrlinger, S. A., Wang, J., Rao, B. Y., Rodriguez, E., Chang, J., Gogos, J., Losonczy, A., & Vitkup, D. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.28.645799 · Cited by 9
Self-citation
Pre- and Post-synaptic Mechanisms of Neuronal Inhibition Assessed Through Biochemically Detailed Modeling of GABA B Receptor Signaling
Mäki‐Marttunen, T., Kismul, J. F., Pajo, K., Schulz, J. M., Manninen, T., Einevoll, G. T., Linne, M., Andreassen, O. A., & Kotaleski, J. H. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0544-25.2025 · Cited by 4
Dynamic Updating of Cognitive Maps via Traces of Experience in the Subiculum
Wang, F., & Bičanski, A. (2026) · Hippocampus · doi:10.1002/hipo.70078 · Cited by 8
Navigation and the efficiency of spatial coding: insights from closed-loop simulations
Ghazinouri, B., Nejad, M. M., & Cheng, S. (2023) · Brain Structure and Function · doi:10.1007/s00429-023-02637-8 · Cited by 3
Disorganized Inhibitory Dynamics in Hippocampal area CA1 of 22q11.2 Deletion Mutant MicePreprint
Herrlinger, S. A., Rao, B. Y., Paredes, M. E. C., Tuttman, A. L., Arain, H., Varol, E., Gogos, J. A., & Losonczy, A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.28.591464 · Cited by 3
Self-citation
Effective connectivity between the medial temporal lobes and early visual cortex modulated by unrestricted viewing predicts memory retrieval and gaze reinstatement
Ladyka‐Wojcik, N., Liu, Z.-X., & Ryan, J. D. (2025) · Imaging Neuroscience · doi:10.1162/imag.a.133 · Cited by 2
The circuitry regulation of associative learning: dissociated and integrated function of the perirhinal cortex and hippocampus
Zhang, J., & Zhang, X. (2026) · Frontiers in Neural Circuits · doi:10.3389/fncir.2026.1789080 · Cited by 3
Self-citation
Learning the Law of Reflection: Event‐Related Potentials of Children Aged 6–12 during Educational Video Game Play
Schroer, J. E., & Thomas, R. D. (2020) · Mind Brain and Education · doi:10.1111/mbe.12259 · Cited by 2
Presubicular VIP expressing interneurons receive facilitating excitation from anterior thalamus
Nassar, M., Richevaux, L., Lim, D., Tayupo, D., Martin, E., & Fricker, D. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.09.032 · Cited by 2
Timing isn’t everything: opposing roles for perisomatic inhibition
Caccavano, A., & McBain, C. J. (2021) · Neuron · doi:10.1016/j.neuron.2021.02.022 · Cited by 2
An Open-Source Virtual Reality System for the Measurement of Spatial Learning in Head-Restrained Mice
Lacefield, C., Cai, H., Ho, H., Dias, C., Chung, H., Hen, R., & Turi, G. F. (2023) · Journal of Visualized Experiments · doi:10.3791/64863 · Cited by 2
Self-citation
Inhibitory neurons: VIP neurons expect rewards
Zou, J., & Hires, S. A. (2023) · Current Biology · doi:10.1016/j.cub.2023.07.059 · Cited by 2
Postweaning Development Influences Endogenous VPAC1 Modulation of LTP Induced by Theta-Burst Stimulation: A Link to Maturation of the Hippocampal GABAergic System
Gil, M., Caulino‐Rocha, A., Bento, M. L., Rodrigues, N. C., Silva‐Cruz, A., Ribeiro, J. A., & Cunha‐Reis, D. (2024) · Biomolecules · doi:10.3390/biom14030379 · Cited by 1
Disinhibition Goes Spatial
Pardi, M. B., Abs, E., & Letzkus, J. J. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.006 · Cited by 2
Medial Entorhinal VIP-expressing interneurons receive direct input from Anterior Dorsal Thalamus and are critical for spatial memoryPreprint
Oulé, M., Badrinarayanan, S., Sundar-Maccagno, R., & Brandon, M. P. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.26.609578 · Cited by 2
Serotonin modulates infraslow oscillation in the dentate gyrus during Non-REM sleepPreprint
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2024) · eLife · doi:10.7554/elife.100196.1 · Cited by 3
Self-citation
Pre- and postsynaptic mechanisms of neuronal inhibition assessed through biochemically detailed modelling of GABAB receptor signallingPreprint
Mäki‐Marttunen, T., Kismul, J. F., Pajo, K., Schulz, J. M., Manninen, T., Einevoll, G. T., Linne, M., Andreassen, O. A., & Kotaleski, J. H. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.19.644198 · Cited by 2
Cell-type-specific encoding of prediction and reward in cortical microcircuits during novelty detectionPreprint
Sharafeldin, A., & Choi, H. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.13.653877 · Cited by 2
Clustered Inputs Maximize Efficiency for Stable Place Field Encoding in Hippocampal Pyramidal NeuronsPreprint
Tasciotti, S., Iascone, D. M., Chavlis, S., Hammond, L. A., Katz, Y., Losonczy, A., Polleux, F., & Poirazi, P. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.30.657022 · Cited by 2
Self-citation
Plasticity in the Olfactory Cortex Is Enabled by Disinhibition of Pyramidal Neuron Apical Dendrites
Loidl, R., & Abs, E. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0892-22.2022 · Cited by 1
Suprachiasmatic Nucleus Vasoactive Intestinal Peptide Neurons Mediate Light-induced Transient Forgetting
Su, X., Tang, Y., Zhong, Y., & Liu, Y. (2025) · Neuroscience Bulletin · doi:10.1007/s12264-025-01456-7 · Cited by 1
Bimodal nonlinear dendrites in PV+ basket cells drive distinct memory-related oscillations
Tzilivaki, A., Larkum, M. E., & Schmitz, D. (2025) · iScience · doi:10.1016/j.isci.2025.113699 · Cited by 1
Crosstalk Between Glycinergic and N-Methyl-D-Aspartate Receptor-Mediated Glutamatergic Transmission in Behaviours Associated with Opioid Use Disorder
Essmat, N., Boldizsár, I., Chalabiani, Y., Varga, B. T., Abbood, S. K., Kirchlechner-Farkas, J. M., Király, K. P., Miklya, I., Gyertyán, I., Tábi, T., et al. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262110526 · Cited by 1
Medial entorhinal VIP-expressing interneurons receive input from the thalamic anterior dorsal nucleus and are critical for spatial memory
Oulé, M., Badrinarayanan, S., Sundar-Maccagno, R., & Brandon, M. P. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2425024122 · Cited by 3
Dysfunctional neural dynamics associated with sensory phenotypes in Fragile X syndrome: insights from mouse models
Goel, A., Razak, K. A., Chubykin, A. A., & Antoine, M. W. (2025) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-025-09634-4 · Cited by 1
Non‐Hebbian Long‐Term Depression at VIP Interneuron Inputs Selectively Tunes Inhibition in Disinhibitory Circuits of Mouse Hippocampus
Jabłońska, J., Wiera, G., & Mozrzymas, J. W. (2026) · Acta Physiologica · doi:10.1111/apha.70162 · Cited by 1
Sublayer‐ and pathway‐specific control of CA1 input processing by VIP interneurons
Iloun, P., Grenier, J., Veillette, F., & Topolnik, L. (2026) · The Journal of Physiology · doi:10.1113/jp291223 · Cited by 1
A cortical–hippocampal communication undergoes rebalancing after new learning
Hall, A. F., & Wang, D. V. (2026) · eLife · doi:10.7554/elife.107370.3 · Cited by 1
Mismatch novelty exploration training shifts VPAC 1 receptor‐mediated modulation of hippocampal synaptic plasticity by endogenous VIP in male rats
Aidil‐Carvalho, F., Caulino‐Rocha, A., Ribeiro, J. A., & Cunha‐Reis, D. (2024) · Journal of Neuroscience Research · doi:10.1002/jnr.25333 · Cited by 1
Mechanisms and implications of high depolarization baseline offsets in conductance-based neuronal models
Kumar, A., Shahul, A. K., & Bhalla, U. S. (2025) · Journal of Neurophysiology · doi:10.1152/jn.00617.2024 · Cited by 1
Intertwining Neuropathogenic Impacts of Aberrant Circadian Rhythm and Impaired Neuroregenerative Plasticity in Huntington’s Disease: Neurotherapeutic Significance of Chemogenetics
Ravichandran, S., Suhasini, R., Deepa, S. M., Selvaraj, D. B., Andrews, J. F. V., Thiagarajan, V., & Kandasamy, M. (2022) · Journal of Molecular Pathology · doi:10.3390/jmp3040030
Synaptic mechanisms underlying the network state-dependent recruitment of VIP-expressing interneuron-specific interneurons in the CA1 hippocampusPreprint
Luo, X., Guet-McCreight, A., Villette, V., Francavilla, R., Marino, B., Chamberland, S., Skinner, F. K., & Topolnik, L. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/433136 · Cited by 1
Behaviorally emergent hippocampal place maps remain stable during memory recallPreprint
Zemla, R., Moore, J. J., & Basu, J. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.08.451449 · Cited by 1
Population dynamics underlying associative learning in the dorsal and ventral hippocampusPreprint
Biane, J. S., Ladow, M. A., Stefanini, F., Boddu, S. P., Fan, A., Hassan, S., Dundar, N., Apodaca-Montano, D. L., Woods, N. I., & Kheirbek, M. A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.16.468862 · Cited by 1
Self-citation
Ventral hippocampal CCK interneurons gate context-reward memoryPreprint
Nguyen, R., Sivakumaran, S., Lambe, E. K., & Kim, J. C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.27.538595 · Cited by 1
Altered firing output of VIP interneurons and early dysfunctions in CA1 hippocampal circuits in the 3xTg mouse model of Alzheimer’s diseasePreprint
Michaud, F., Francavilla, R., Topolnik, D., Iloun, P., Tamboli, S., Calon, F., & Topolnik, L. (2024) · eLife · doi:10.7554/elife.95412.1 · Cited by 1
behaviorMate: An Intranet of Things Approach for Adaptable Control of Behavioral and Navigation-Based ExperimentsPreprint
Bowler, J. C., Zakka, G., Yong, H. C., Li, W., Rao, B. Y., Liao, Z., Priestley, J. B., & Losonczy, A. (2024) · doi:10.7554/elife.97433.1 · Cited by 1
Self-citation
Serotonin modulates infraslow oscillation in the dentate gyrus during Non-REM sleepPreprint
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2025) · eLife · doi:10.7554/elife.100196.2 · Cited by 1
Self-citation
Learning reorganizes dendritic and stabilizes axonal initial segment inhibitory synapses in CA1 pyramidal neuronsPreprint
Klimmt, H., Kappel, D., Ulivi, A. F., Argunşah, A. Ö., Murthy, B., Somatakis, S., Huettl, R.-E., Remy, S., & Attardo, A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.04.641429 · Cited by 1
Navigational Frames of Reference as Critical Regulators of Hippocampal Interneuron Coding PropertiesPreprint
Bott, J.-B., Penazzi, L., Al-Achkar, S., Cho, M., Rivard, B., Gauthier-Lafrenière, E., & Williams, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.07.637101 · Cited by 1
Breaking Balance: Encoding local error signals in perturbations of excitation-inhibition balancePreprint
Rossbroich, J., & Zenke, F. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.12.653626 · Cited by 2
Cortical dissociation of spatial reference frames during place navigationPreprint
LaChance, P. A., Gross, E. R., Sankaranarayanan, S., & Hasselmo, M. E. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.25.661569 · Cited by 1
Hippocampal neuronal and astrocytic responses to noradrenaline and natural arousalPreprint
Duss, S. N., Wilhelm, M., Marinescu, A., Zhang, R., Helmchen, F., Bohacek, J., & Rupprecht, P. (2026) · eLife · doi:10.7554/elife.111593.1 · Cited by 3
Place and behavioral modulation of hippocampal neurons during immobility
Sartorato, N., Zouridis, I. S., Narantsatsralt, U.-U., Blanco-Hernández, E., & Burgalossi, A. (2026) · Nature Communications · doi:10.1038/s41467-026-75492-w · Cited by 1
“39 – 41).”
Guardians of the learning gate
Hegedüs, P., Martínez‐Bellver, S., & Hangya, B. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0519-8
Neural circuit dynamics of drug-context associative learning in the hippocampusPreprint
Sun, Y., & Giocomo, L. M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.02.458796
Compartment-specific tuning of hippocampal dendritic feature selectivity by intracellular Ca 2+ releasePreprint
O’Hare, J. K., Hirabayashi, Y., Hewitt, V. L., Blockus, H., Szoboszlay, M., Rolotti, S. V., Geiller, T. C., Negrean, A., Chelur, V., Losonczy, A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.27.460811
Self-citation
Interneuron switching on and off across memory rhythms
Tzilivaki, A., Maier, N., & Schmitz, D. (2022) · Neuron · doi:10.1016/j.neuron.2022.05.019
mTORC1-mediated acquisition of reward-related spatial representations by hippocampal somatostatin interneuronsaPreprint
Michon, F.-X., Laplante, I., Bosson, A., Robitaille, R., & Lacaille, J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.24.529922
Functional networks of inhibitory neurons orchestrate synchrony in the hippocampusPreprint
Cossart, R., Bocchio, M., Vorobyev, A., Sadeh, S., Brustlein, S., Reichinnek, S., Emiliani, V., Claudia Clopath, A., & Dard, R. F. (2023) · Research Square · doi:10.21203/rs.3.rs-3304483/v1
Altered firing output of VIP interneurons and early dysfunctions in CA1 hippocampal circuits in the 3xTg mouse model of Alzheimer’s diseasePreprint
Michaud, F., Francavilla, R., Topolnik, D., Iloun, P., Tamboli, S., Calon, F., & Topolnik, L. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.12.575331
Two Types of Presubicular Vip Expressing Interneurons Receive Facilitating Excitation from Anterior ThalamusPreprint
Nassar, M., Richevaux, L., Lim, D., Tayupo, D., Martin, E., & Fricker, D. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4736244
Additional file 5 of mTORC1-mediated acquisition of reward-related representations by hippocampal somatostatin interneurons
Michon, F.-X., Laplante, I., Bosson, A., Robitaille, R., & Lacaille, J. (2023) · Figshare · doi:10.6084/m9.figshare.23621571
Reviewer #1 (Public Review): behaviorMate: An Intranet of Things Approach for Adaptable Control of Behavioral and Navigation-Based Experiments
(2024) · doi:10.7554/elife.97433.1.sa2
Reviewer #2 (Public Review): behaviorMate: An Intranet of Things Approach for Adaptable Control of Behavioral and Navigation-Based Experiments
(2024) · doi:10.7554/elife.97433.1.sa1
Reviewer #3 (Public Review): behaviorMate: An Intranet of Things Approach for Adaptable Control of Behavioral and Navigation-Based Experiments
(2024) · doi:10.7554/elife.97433.1.sa0
Author response: behaviorMate: An Intranet of Things Approach for Adaptable Control of Behavioral and Navigation-Based Experiments
Bowler, J. C., Zakka, G., Yong, H. C., Li, W., Rao, B. Y., Liao, Z., Priestley, J. B., & Losonczy, A. (2024) · doi:10.7554/elife.97433.1.sa4
Self-citation
eLife Assessment: behaviorMate: An Intranet of Things Approach for Adaptable Control of Behavioral and Navigation-Based Experiments
Kemere, C. T. (2024) · doi:10.7554/elife.97433.1.sa3
Altered firing output of VIP interneurons and early dysfunctions in CA1 hippocampal circuits in the 3xTg mouse model of Alzheimer’s diseasePreprint
Michaud, F., Francavilla, R., Topolnik, D., Iloun, P., Tamboli, S., Calon, F., & Topolnik, L. (2024) · eLife · doi:10.7554/elife.95412.2
Altered firing output of VIP interneurons and early dysfunctions in CA1 hippocampal circuits in the 3xTg mouse model of Alzheimer’s disease
Michaud, F., Francavilla, R., Topolnik, D., Iloun, P., Tamboli, S., Calon, F., & Topolnik, L. (2024) · eLife · doi:10.7554/elife.95412.3
Interneurons in learning and memory
Campos‐Cardoso, R., Desa, Z. R., Fitzgerald, B. L., Franks, H. T., Gonçalez, J. L., & Cummings, K. A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00055-9
Representation of spatial information in the CA1 field
Mysin, I. E., Vasilev, A. O., Dubrovin, S. V., & Skorokhod, S. N. (2024) · Журнал высшей нервной деятельности им И П Павлова · doi:10.31857/s0044467724050019
behaviorMate: An Intranet of Things Approach for Adaptable Control of Behavioral and Navigation-Based ExperimentsPreprint
Bowler, J. C., Zakka, G., Yong, H. C., Li, W., Rao, B. Y., Liao, Z., Priestley, J. B., & Losonczy, A. (2025) · doi:10.7554/elife.97433.2
Self-citation
Local Circuits
Grosmark, A., Milstein, A. D., Losonczy, A., & Soltész, I. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0007
Self-citation
Serotonin modulates infraslow oscillation in the dentate gyrus during Non-REM sleepPreprint
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2025) · eLife · doi:10.7554/elife.100196.3 · Cited by 1
Self-citation
Representation of Spatial Information in Field CA1
Mysin, I. E., Vasilev, A. O., Dubrovin, S. V., & Skorokhod, S. N. (2025) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-025-01783-2
Graded remapping of prefrontal representations preserves a cumulative record of distinct events within an environment
Chen, Y. K., Tu, G., Zhang, L., & Takehara‐Nishiuchi, K. (2025) · iScience · doi:10.1016/j.isci.2025.113009
Role and mechanisms of interneurons in chronic pain and pain-induced cognitive impairment.
Wang, Q., Zhang, G.-F., & Wang, B. (2025) · PubMed Central · doi:10.11817/j.issn.1672-7347.2025.240402
Hippocampal sequences traverse a memory spacePreprint
Ulrich, O. C., Gomez, D. M., Lane, M. R., & Priestley, J. B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.21.689701
Self-citation
Additional file 3 of mTORC1-mediated acquisition of reward-related representations by hippocampal somatostatin interneurons
Michon, F.-X., Laplante, I., Bosson, A., Robitaille, R., & Lacaille, J. (2023) · Figshare · doi:10.6084/m9.figshare.23621565
Additional file 2 of mTORC1-mediated acquisition of reward-related representations by hippocampal somatostatin interneurons
Michon, F.-X., Laplante, I., Bosson, A., Robitaille, R., & Lacaille, J. (2023) · Figshare · doi:10.6084/m9.figshare.23621562
Additional file 1 of mTORC1-mediated acquisition of reward-related representations by hippocampal somatostatin interneurons
Michon, F.-X., Laplante, I., Bosson, A., Robitaille, R., & Lacaille, J. (2023) · Figshare · doi:10.6084/m9.figshare.23621559
Additional file 4 of mTORC1-mediated acquisition of reward-related representations by hippocampal somatostatin interneurons
Michon, F.-X., Laplante, I., Bosson, A., Robitaille, R., & Lacaille, J. (2023) · Figshare · doi:10.6084/m9.figshare.23621568

Authors: Turi, 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., Zemelman, B. V., Poirazi, P., & Losonczy, A.
Affiliations: Columbia University (US)
Mortimer B. Zuckerman Mind Brain Behavior Institute (US)
FORTH Institute of Molecular Biology and Biotechnology (GR)
University of Crete (GR)
The University of Texas at Austin (US)
Corresponding author: Poirazi, Panayiota
Losonczy, Attila
ORCID: Turi, Gergely Farkas
Chavlis, Spyridon
Pandi, Ioanna
O’Hare, Justin
Priestley, James Benjamin
Grosmark, Andres Daniel
Liao, Zhenrui
Ladow, Max
Zhang, Jeff Fang
Zemelman, Boris Valery
Poirazi, Panayiota
Losonczy, Attila
Venue: Neuron
Publisher: Elsevier BV
Published: 2019-03
Volume: 101
Issue: 6
Pages: 1150-1165.e8
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2019.01.009
PMC: PMC6428605
OpenAlex: W2913259775
Cited by: 218
References: 82
Citations by year: 2026: 26 · 2025: 35 · 2024: 34 · 2023: 33 · 2022: 30 · 2021: 27 · 2020: 22 · 2019: 9
FWCI: 12.79
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, 385 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (1R01MH100631)
National Institute of Neurological Disorders and Stroke (1U19NS104590, 1R01NS094668)
Zegar Family Foundation Award
Kavli Foundation (NYSTEM-C029157, S10 OD018464)
NIMH (F32MH118716)
Revson Foundation
NINDS (U01NS094330, U01NS099720)
ERC Starting Grant dEMORY (ERC-2012-StG-311435)
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: vasoactive intestinal peptide, GABAergic interneurons, hippocampal CA1, goal-directed learning, spatial learning, spatial navigation, two-photon calcium imaging, optogenetics, computational modeling, foraging behavior, behavioral state
MeSH terms: Animals, Appetitive Behavior, Goals, Hippocampus, Interneurons, Neural Inhibition, Vasoactive Intestinal Peptide, Pyramidal Cells, Neocortex, Mice, CA1 Region, Hippocampal, Optogenetics, Spatial Learning

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

Vasoactive Intestinal Polypeptide-Expressing Interneurons in the Hippocampus Support Goal-Oriented Spatial Learning

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks