VIP Interneurons in Mouse Primary Visual Cortex Selectively Enhance Responses to Weak but Specific Stimuli

Overview

Journal Elife

Specialty Biology

Date 2020 Oct 27

PMID 33108272

Citations 36

Authors

Daniel J Millman

Gabriel Koch Ocker

Shiella Caldejon

India Kato

Josh D Larkin

Eric Kenji Lee

Jennifer Luviano

Chelsea Nayan

Thuyanh V Nguyen

Kat North

Sam Seid

Cassandra White

Jerome Lecoq

Clay Reid

Michael A Buice

Saskia Ej de Vries

Affiliations

Soon will be listed here.

Abstract

Vasoactive intestinal peptide-expressing (VIP) interneurons in the cortex regulate feedback inhibition of pyramidal neurons through suppression of somatostatin-expressing (SST) interneurons and, reciprocally, SST neurons inhibit VIP neurons. Although VIP neuron activity in the primary visual cortex (V1) of mouse is highly correlated with locomotion, the relevance of locomotion-related VIP neuron activity to visual coding is not known. Here we show that VIP neurons in mouse V1 respond strongly to low contrast front-to-back motion that is congruent with self-motion during locomotion but are suppressed by other directions and contrasts. VIP and SST neurons have complementary contrast tuning. Layer 2/3 contains a substantially larger population of low contrast preferring pyramidal neurons than deeper layers, and layer 2/3 (but not deeper layer) pyramidal neurons show bias for front-to-back motion specifically at low contrast. Network modeling indicates that VIP-SST mutual antagonism regulates the gain of the cortex to achieve sensitivity to specific weak stimuli without compromising network stability.

Citing Articles

Context-Sensitive Conscious Interpretation and Layer-5 Pyramidal Neurons in Multistable Perception.

Bachmann T Brain Behav. 2025; 15(3):e70393.

PMID: 40038853 PMC: 11879900. DOI: 10.1002/brb3.70393.

Optogenetic restoration of neuron subtype-specific cortical activity ameliorates motor deficits in Huntington's Disease mice.

Blumenstock S, Arakelyan D, Del Grosso N, Schneider S, Shao Y, Gjoni E bioRxiv. 2025; .

PMID: 39974900 PMC: 11839025. DOI: 10.1101/2025.02.07.637155.

Interneuronal modulations as a functional switch for cortical computations: mechanisms and implication for disease.

Zerlaut Y, Tzilivaki A Front Cell Neurosci. 2025; 18:1479579.

PMID: 39916937 PMC: 11799556. DOI: 10.3389/fncel.2024.1479579.

Ensemble priming via competitive inhibition: local mechanisms of sensory context storage and deviance detection in the neocortical column.

Thorpe R, Moore C, Jones S bioRxiv. 2025; .

PMID: 39829817 PMC: 11741386. DOI: 10.1101/2025.01.08.631952.

The gamma rhythm as a guardian of brain health.

Ichim A, Barzan H, Moca V, Nagy-Dabacan A, Ciuparu A, Hapca A Elife. 2024; 13.

PMID: 39565646 PMC: 11578591. DOI: 10.7554/eLife.100238.

References

Dipoppa M, Ranson A, Krumin M, Pachitariu M, Carandini M, Harris K . Vision and Locomotion Shape the Interactions between Neuron Types in Mouse Visual Cortex. Neuron. 2018; 98(3):602-615.e8. PMC: 5946730. DOI: 10.1016/j.neuron.2018.03.037. View

Adesnik H . Synaptic Mechanisms of Feature Coding in the Visual Cortex of Awake Mice. Neuron. 2017; 95(5):1147-1159.e4. PMC: 5580349. DOI: 10.1016/j.neuron.2017.08.014. View

Ahmadian Y, Rubin D, Miller K . Analysis of the stabilized supralinear network. Neural Comput. 2013; 25(8):1994-2037. PMC: 4026108. DOI: 10.1162/NECO_a_00472. View

Kraynyukova N, Tchumatchenko T . Stabilized supralinear network can give rise to bistable, oscillatory, and persistent activity. Proc Natl Acad Sci U S A. 2018; 115(13):3464-3469. PMC: 5879648. DOI: 10.1073/pnas.1700080115. View

Roux L, Buzsaki G . Tasks for inhibitory interneurons in intact brain circuits. Neuropharmacology. 2014; 88:10-23. PMC: 4254329. DOI: 10.1016/j.neuropharm.2014.09.011. View

Scala F, Kobak D, Shan S, Bernaerts Y, Laturnus S, Cadwell C . Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas. Nat Commun. 2019; 10(1):4174. PMC: 6744474. DOI: 10.1038/s41467-019-12058-z. View

Carandini M, Heeger D . Normalization as a canonical neural computation. Nat Rev Neurosci. 2011; 13(1):51-62. PMC: 3273486. DOI: 10.1038/nrn3136. View

Sanzeni A, Akitake B, Goldbach H, Leedy C, Brunel N, Histed M . Inhibition stabilization is a widespread property of cortical networks. Elife. 2020; 9. PMC: 7324160. DOI: 10.7554/eLife.54875. View

Rubin D, Van Hooser S, Miller K . The stabilized supralinear network: a unifying circuit motif underlying multi-input integration in sensory cortex. Neuron. 2015; 85(2):402-17. PMC: 4344127. DOI: 10.1016/j.neuron.2014.12.026. View

10.

Priebe N, Ferster D . Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron. 2008; 57(4):482-97. DOI: 10.1016/j.neuron.2008.02.005. View

11.

Tremblay R, Lee S, Rudy B . GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits. Neuron. 2016; 91(2):260-92. PMC: 4980915. DOI: 10.1016/j.neuron.2016.06.033. View

12.

Liu L, Miller K, Pack C . A Unifying Motif for Spatial and Directional Surround Suppression. J Neurosci. 2017; 38(4):989-999. PMC: 5783971. DOI: 10.1523/JNEUROSCI.2386-17.2017. View

13.

Cone J, Scantlen M, Histed M, Maunsell J . Different Inhibitory Interneuron Cell Classes Make Distinct Contributions to Visual Contrast Perception. eNeuro. 2019; 6(1). PMC: 6414440. DOI: 10.1523/ENEURO.0337-18.2019. View

14.

Huang L, Ledochowitsch P, Knoblich U, Lecoq J, Murphy G, Reid R . Relationship between simultaneously recorded spiking activity and fluorescence signal in GCaMP6 transgenic mice. Elife. 2021; 10. PMC: 8060029. DOI: 10.7554/eLife.51675. View

15.

Glickfeld L, Histed M, Maunsell J . Mouse primary visual cortex is used to detect both orientation and contrast changes. J Neurosci. 2013; 33(50):19416-22. PMC: 3858618. DOI: 10.1523/JNEUROSCI.3560-13.2013. View

16.

Linaro D, Ocker G, Doiron B, Giugliano M . Correlation Transfer by Layer 5 Cortical Neurons Under Recreated Synaptic Inputs . J Neurosci. 2019; 39(39):7648-7663. PMC: 6764207. DOI: 10.1523/JNEUROSCI.3169-18.2019. View

17.

Cruikshank S, Urabe H, Nurmikko A, Connors B . Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron. 2010; 65(2):230-45. PMC: 2826223. DOI: 10.1016/j.neuron.2009.12.025. View

18.

Albrecht D, Geisler W, Frazor R, Crane A . Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function. J Neurophysiol. 2002; 88(2):888-913. DOI: 10.1152/jn.2002.88.2.888. View

19.

de Vries S, Lecoq J, Buice M, Groblewski P, Ocker G, Oliver M . A large-scale standardized physiological survey reveals functional organization of the mouse visual cortex. Nat Neurosci. 2019; 23(1):138-151. PMC: 6948932. DOI: 10.1038/s41593-019-0550-9. View

20.

Jewell S, Hocking T, Fearnhead P, Witten D . Fast nonconvex deconvolution of calcium imaging data. Biostatistics. 2019; 21(4):709-726. PMC: 7566556. DOI: 10.1093/biostatistics/kxy083. View