Recruitment of GABAergic Interneurons in the Barrel Cortex During Active Tactile Behavior

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2019 Aug 31

PMID 31466734

Citations 81

Authors

Jianing Yu

Hang Hu

Ariel Agmon

Karel Svoboda

Affiliations

Soon will be listed here.

Abstract

Neural computation involves diverse types of GABAergic inhibitory interneurons that are integrated with excitatory (E) neurons into precisely structured circuits. To understand how each neuron type shapes sensory representations, we measured firing patterns of defined types of neurons in the barrel cortex while mice performed an active, whisker-dependent object localization task. Touch excited fast-spiking (FS) interneurons at short latency, followed by activation of E neurons and somatostatin-expressing (SST) interneurons. Touch only weakly modulated vasoactive intestinal polypeptide-expressing (VIP) interneurons. Voluntary whisker movement activated FS neurons in the ventral posteromedial nucleus (VPM) target layers, a subset of SST neurons and a majority of VIP neurons. Together, FS neurons track thalamic input, mediating feedforward inhibition. SST neurons monitor local excitation, providing feedback inhibition. VIP neurons are activated by non-sensory inputs, disinhibiting E and FS neurons. Our data reveal rules of recruitment for interneuron types during behavior, providing foundations for understanding computation in cortical microcircuits.

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References

Jiang X, Shen S, Cadwell C, Berens P, Sinz F, Ecker A . Principles of connectivity among morphologically defined cell types in adult neocortex. Science. 2015; 350(6264):aac9462. PMC: 4809866. DOI: 10.1126/science.aac9462. View

Hioki H, Okamoto S, Konno M, Kameda H, Sohn J, Kuramoto E . Cell type-specific inhibitory inputs to dendritic and somatic compartments of parvalbumin-expressing neocortical interneuron. J Neurosci. 2013; 33(2):544-55. PMC: 6704929. DOI: 10.1523/JNEUROSCI.2255-12.2013. View

Wilent W, Contreras D . Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci. 2005; 8(10):1364-70. DOI: 10.1038/nn1545. View

Staiger J, Zilles K, Freund T . Innervation of VIP-immunoreactive neurons by the ventroposteromedial thalamic nucleus in the barrel cortex of the rat. J Comp Neurol. 1996; 367(2):194-204. DOI: 10.1002/(SICI)1096-9861(19960401)367:2<194::AID-CNE3>3.0.CO;2-0. View

Petreanu L, Mao T, Sternson S, Svoboda K . The subcellular organization of neocortical excitatory connections. Nature. 2009; 457(7233):1142-5. PMC: 2745650. DOI: 10.1038/nature07709. View

Mehta S, Whitmer D, Figueroa R, Williams B, Kleinfeld D . Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol. 2007; 5(2):e15. PMC: 1769422. DOI: 10.1371/journal.pbio.0050015. View

de Kock C, Bruno R, Spors H, Sakmann B . Layer- and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J Physiol. 2007; 581(Pt 1):139-54. PMC: 2075227. DOI: 10.1113/jphysiol.2006.124321. View

Beierlein M, Gibson J, Connors B . Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol. 2003; 90(5):2987-3000. DOI: 10.1152/jn.00283.2003. View

Kinnischtzke A, Simons D, Fanselow E . Motor cortex broadly engages excitatory and inhibitory neurons in somatosensory barrel cortex. Cereb Cortex. 2013; 24(8):2237-48. PMC: 4148616. DOI: 10.1093/cercor/bht085. View

10.

Naka A, Veit J, Shababo B, Chance R, Risso D, Stafford D . Complementary networks of cortical somatostatin interneurons enforce layer specific control. Elife. 2019; 8. PMC: 6422636. DOI: 10.7554/eLife.43696. View

11.

Hooks B, Hires S, Zhang Y, Huber D, Petreanu L, Svoboda K . Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol. 2011; 9(1):e1000572. PMC: 3014926. DOI: 10.1371/journal.pbio.1000572. View

12.

Agmon A, Connors B . Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience. 1991; 41(2-3):365-79. DOI: 10.1016/0306-4522(91)90333-j. View

13.

Pinault D . A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Methods. 1996; 65(2):113-36. DOI: 10.1016/0165-0270(95)00144-1. View

14.

Constantinople C, Bruno R . Deep cortical layers are activated directly by thalamus. Science. 2013; 340(6140):1591-4. PMC: 4203320. DOI: 10.1126/science.1236425. View

15.

Gentet L, Avermann M, Matyas F, Staiger J, Petersen C . Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron. 2010; 65(3):422-35. DOI: 10.1016/j.neuron.2010.01.006. View

16.

Agmon A, Connors B . Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci. 1992; 12(1):319-29. PMC: 6575688. View

17.

Oliva Jr A, Jiang M, Lam T, Smith K, Swann J . Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci. 2000; 20(9):3354-68. PMC: 6773106. View

18.

Hong Y, Lacefield C, Rodgers C, Bruno R . Sensation, movement and learning in the absence of barrel cortex. Nature. 2018; 561(7724):542-546. PMC: 6173956. DOI: 10.1038/s41586-018-0527-y. View

19.

Lefort S, Tomm C, Sarria J, Petersen C . The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron. 2009; 61(2):301-16. DOI: 10.1016/j.neuron.2008.12.020. View

20.

Gentet L, Kremer Y, Taniguchi H, Huang Z, Staiger J, Petersen C . Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci. 2012; 15(4):607-12. DOI: 10.1038/nn.3051. View