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

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2019 Feb 5

PMID 30713030

Citations 89

Authors

Gergely Farkas Turi

Wen-Ke Li

Spyridon Chavlis

Ioanna Pandi

Justin OHare

James Benjamin Priestley

Andres Daniel Grosmark

Zhenrui Liao

Max Ladow

Jeff Fang Zhang

Boris Valery Zemelman

Panayiota Poirazi

Attila Losonczy

Affiliations

Soon will be listed here.

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.

Citing Articles

Inhibitory and disinhibitory VIP IN-mediated circuits in neocortex.

Dellal S, Zurita H, Valero M, Abad-Perez P, Kruglikov I, Meng J bioRxiv. 2025; .

PMID: 40060562 PMC: 11888407. DOI: 10.1101/2025.02.26.640383.

Brain-wide presynaptic networks of functionally distinct cortical neurons.

Inacio A, Lam K, Zhao Y, Pereira F, Gerfen C, Lee S Nature. 2025; .

PMID: 40011781 DOI: 10.1038/s41586-025-08631-w.

An of Things approach for adaptable control of behavioral and navigation-based experiments.

Bowler J, Zakka G, Yong H, Li W, Rao B, Liao Z Elife. 2025; 13.

PMID: 40008867 PMC: 11867614. DOI: 10.7554/eLife.97433.

Functional networks of inhibitory neurons orchestrate synchrony in the hippocampus.

Bocchio M, Vorobyev A, Sadeh S, Brustlein S, Dard R, Reichinnek S PLoS Biol. 2024; 22(10):e3002837.

PMID: 39401246 PMC: 11501041. DOI: 10.1371/journal.pbio.3002837.

Distinct ventral hippocampal inhibitory microcircuits regulating anxiety and fear behaviors.

Li K, Koukoutselos K, Sakaguchi M, Ciocchi S Nat Commun. 2024; 15(1):8228.

PMID: 39300067 PMC: 11413373. DOI: 10.1038/s41467-024-52466-4.

References

Jia H, Rochefort N, Chen X, Konnerth A . In vivo two-photon imaging of sensory-evoked dendritic calcium signals in cortical neurons. Nat Protoc. 2011; 6(1):28-35. DOI: 10.1038/nprot.2010.169. View

Dombeck D, Khabbaz A, Collman F, Adelman T, Tank D . Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron. 2007; 56(1):43-57. PMC: 2268027. DOI: 10.1016/j.neuron.2007.08.003. View

Solstad T, Moser E, Einevoll G . From grid cells to place cells: a mathematical model. Hippocampus. 2006; 16(12):1026-31. DOI: 10.1002/hipo.20244. View

Harris K, Csicsvari J, Hirase H, Dragoi G, Buzsaki G . Organization of cell assemblies in the hippocampus. Nature. 2003; 424(6948):552-6. DOI: 10.1038/nature01834. View

Pinto L, Dan Y . Cell-Type-Specific Activity in Prefrontal Cortex during Goal-Directed Behavior. Neuron. 2015; 87(2):437-50. PMC: 4506259. DOI: 10.1016/j.neuron.2015.06.021. View

Zaremba J, Diamantopoulou A, Danielson N, Grosmark A, Kaifosh P, Bowler J . Impaired hippocampal place cell dynamics in a mouse model of the 22q11.2 deletion. Nat Neurosci. 2017; 20(11):1612-1623. PMC: 5763006. DOI: 10.1038/nn.4634. View

Marshall L, Henze D, Hirase H, Leinekugel X, Dragoi G, Buzsaki G . Hippocampal pyramidal cell-interneuron spike transmission is frequency dependent and responsible for place modulation of interneuron discharge. J Neurosci. 2002; 22(2):RC197. PMC: 6758681. View

Ego-Stengel V, Wilson M . Spatial selectivity and theta phase precession in CA1 interneurons. Hippocampus. 2006; 17(2):161-74. DOI: 10.1002/hipo.20253. View

Chamberland S, Topolnik L . Inhibitory control of hippocampal inhibitory neurons. Front Neurosci. 2012; 6:165. PMC: 3496901. DOI: 10.3389/fnins.2012.00165. View

10.

Del Pino I, Brotons-Mas J, Marques-Smith A, Marighetto A, Frick A, Marin O . Abnormal wiring of CCK basket cells disrupts spatial information coding. Nat Neurosci. 2017; 20(6):784-792. PMC: 5446788. DOI: 10.1038/nn.4544. View

11.

Arriaga M, Han E . Dedicated Hippocampal Inhibitory Networks for Locomotion and Immobility. J Neurosci. 2017; 37(38):9222-9238. PMC: 6596740. DOI: 10.1523/JNEUROSCI.1076-17.2017. View

12.

Hok V, Lenck-Santini P, Roux S, Save E, Muller R, Poucet B . Goal-related activity in hippocampal place cells. J Neurosci. 2007; 27(3):472-82. PMC: 6672791. DOI: 10.1523/JNEUROSCI.2864-06.2007. View

13.

Poirazi P, Brannon T, Mel B . Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron. 2003; 37(6):977-87. DOI: 10.1016/s0896-6273(03)00148-x. View

14.

Bittner K, Milstein A, Grienberger C, Romani S, Magee J . Behavioral time scale synaptic plasticity underlies CA1 place fields. Science. 2017; 357(6355):1033-1036. PMC: 7289271. DOI: 10.1126/science.aan3846. View

15.

Gauthier J, Tank D . A Dedicated Population for Reward Coding in the Hippocampus. Neuron. 2018; 99(1):179-193.e7. PMC: 7023678. DOI: 10.1016/j.neuron.2018.06.008. View

16.

Caroni P . Inhibitory microcircuit modules in hippocampal learning. Curr Opin Neurobiol. 2015; 35:66-73. DOI: 10.1016/j.conb.2015.06.010. View

17.

Danielson N, Zaremba J, Kaifosh P, Bowler J, Ladow M, Losonczy A . Sublayer-Specific Coding Dynamics during Spatial Navigation and Learning in Hippocampal Area CA1. Neuron. 2016; 91(3):652-65. PMC: 4975984. DOI: 10.1016/j.neuron.2016.06.020. View

18.

David C, Schleicher A, Zuschratter W, Staiger J . The innervation of parvalbumin-containing interneurons by VIP-immunopositive interneurons in the primary somatosensory cortex of the adult rat. Eur J Neurosci. 2007; 25(8):2329-40. DOI: 10.1111/j.1460-9568.2007.05496.x. View

19.

Fishell G, Rudy B . Mechanisms of inhibition within the telencephalon: "where the wild things are". Annu Rev Neurosci. 2011; 34:535-67. PMC: 3556485. DOI: 10.1146/annurev-neuro-061010-113717. View

20.

Sheffield M, Adoff M, Dombeck D . Increased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation. Neuron. 2017; 96(2):490-504.e5. PMC: 5642299. DOI: 10.1016/j.neuron.2017.09.029. View