Layer-Specific Physiological Features and Interlaminar Interactions in the Primary Visual Cortex of the Mouse

Yuta Senzai; Antonio Fernandez-Ruiz; György Buzsáki

doi:10.1016/j.neuron.2018.12.009

Layer-Specific Physiological Features and Interlaminar Interactions in the Primary Visual Cortex of the Mouse

Yuta Senzai, Antonio Fernandez-Ruiz, György Buzsáki^*

^*Corresponding author for this work

Neuroscience

Research output: Contribution to journal › Article › peer-review

152 Scopus citations

Abstract

The relationship between mesoscopic local field potentials (LFPs) and single-neuron firing in the multi-layered neocortex is poorly understood. Simultaneous recordings from all layers in the primary visual cortex (V1) of the behaving mouse revealed functionally defined layers in V1. The depth of maximum spike power and sink-source distributions of LFPs provided consistent laminar landmarks across animals. Coherence of gamma oscillations (30–100 Hz) and spike-LFP coupling identified six physiological layers and further sublayers. Firing rates, burstiness, and other electrophysiological features of neurons displayed unique layer and brain state dependence. Spike transmission strength from layer 2/3 cells to layer 5 pyramidal cells and interneurons was stronger during waking compared with non-REM sleep but stronger during non-REM sleep among deep-layer excitatory neurons. A subset of deep-layer neurons was active exclusively in the DOWN state of non-REM sleep. These results bridge mesoscopic LFPs and single-neuron interactions with laminar structure in V1.

Original language	English (US)
Pages (from-to)	500-513.e5
Journal	Neuron
Volume	101
Issue number	3
DOIs	https://doi.org/10.1016/j.neuron.2018.12.009
State	Published - Feb 6 2019

Funding

We thank Sam McKenzie, Daniel Levenstein, Patrick Reeson, Guy Bouvier, Riccardo Beltramo, Massimo Scanziani, Robert Shapley, Rachel Swanson, Manuel Valero, and Viktor Varga for comments on the manuscript. This work was supported by the Nakajima Foundation (Y.S.); grants MH54671 , MH107396 , and NS090583 from the NIH (G.B.) and grants 1545858 and 1707316 from the National Science Foundation (to Euisik Yoon); and a Sir Henry Wellcome Postdoctoral Fellowship (A.F.-R.). We thank Sam McKenzie, Daniel Levenstein, Patrick Reeson, Guy Bouvier, Riccardo Beltramo, Massimo Scanziani, Robert Shapley, Rachel Swanson, Manuel Valero, and Viktor Varga for comments on the manuscript. This work was supported by the Nakajima Foundation (Y.S.); grants MH54671, MH107396, and NS090583 from the NIH (G.B.) and grants 1545858 and 1707316 from the National Science Foundation (to Euisik Yoon); and a Sir Henry Wellcome Postdoctoral Fellowship (A.F.-R.).

Keywords

alpha rhythm
cell types
cortical layers
current source density
laminar recordings
optogenetics
oscillations
primary visual cortex
sleep

ASJC Scopus subject areas

General Neuroscience

Access to Document

10.1016/j.neuron.2018.12.009

Cite this

@article{a025128be250404cb1b5fc4f14bf23bd,

title = "Layer-Specific Physiological Features and Interlaminar Interactions in the Primary Visual Cortex of the Mouse",

abstract = "The relationship between mesoscopic local field potentials (LFPs) and single-neuron firing in the multi-layered neocortex is poorly understood. Simultaneous recordings from all layers in the primary visual cortex (V1) of the behaving mouse revealed functionally defined layers in V1. The depth of maximum spike power and sink-source distributions of LFPs provided consistent laminar landmarks across animals. Coherence of gamma oscillations (30–100 Hz) and spike-LFP coupling identified six physiological layers and further sublayers. Firing rates, burstiness, and other electrophysiological features of neurons displayed unique layer and brain state dependence. Spike transmission strength from layer 2/3 cells to layer 5 pyramidal cells and interneurons was stronger during waking compared with non-REM sleep but stronger during non-REM sleep among deep-layer excitatory neurons. A subset of deep-layer neurons was active exclusively in the DOWN state of non-REM sleep. These results bridge mesoscopic LFPs and single-neuron interactions with laminar structure in V1.",

keywords = "alpha rhythm, cell types, cortical layers, current source density, laminar recordings, optogenetics, oscillations, primary visual cortex, sleep",

author = "Yuta Senzai and Antonio Fernandez-Ruiz and Gy{\"o}rgy Buzs{\'a}ki",

note = "Publisher Copyright: {\textcopyright} 2019 The Authors",

year = "2019",

month = feb,

day = "6",

doi = "10.1016/j.neuron.2018.12.009",

language = "English (US)",

volume = "101",

pages = "500--513.e5",

journal = "Neuron",

issn = "0896-6273",

publisher = "Cell Press",

number = "3",

}

TY - JOUR

T1 - Layer-Specific Physiological Features and Interlaminar Interactions in the Primary Visual Cortex of the Mouse

AU - Senzai, Yuta

AU - Fernandez-Ruiz, Antonio

AU - Buzsáki, György

PY - 2019/2/6

Y1 - 2019/2/6

N2 - The relationship between mesoscopic local field potentials (LFPs) and single-neuron firing in the multi-layered neocortex is poorly understood. Simultaneous recordings from all layers in the primary visual cortex (V1) of the behaving mouse revealed functionally defined layers in V1. The depth of maximum spike power and sink-source distributions of LFPs provided consistent laminar landmarks across animals. Coherence of gamma oscillations (30–100 Hz) and spike-LFP coupling identified six physiological layers and further sublayers. Firing rates, burstiness, and other electrophysiological features of neurons displayed unique layer and brain state dependence. Spike transmission strength from layer 2/3 cells to layer 5 pyramidal cells and interneurons was stronger during waking compared with non-REM sleep but stronger during non-REM sleep among deep-layer excitatory neurons. A subset of deep-layer neurons was active exclusively in the DOWN state of non-REM sleep. These results bridge mesoscopic LFPs and single-neuron interactions with laminar structure in V1.

AB - The relationship between mesoscopic local field potentials (LFPs) and single-neuron firing in the multi-layered neocortex is poorly understood. Simultaneous recordings from all layers in the primary visual cortex (V1) of the behaving mouse revealed functionally defined layers in V1. The depth of maximum spike power and sink-source distributions of LFPs provided consistent laminar landmarks across animals. Coherence of gamma oscillations (30–100 Hz) and spike-LFP coupling identified six physiological layers and further sublayers. Firing rates, burstiness, and other electrophysiological features of neurons displayed unique layer and brain state dependence. Spike transmission strength from layer 2/3 cells to layer 5 pyramidal cells and interneurons was stronger during waking compared with non-REM sleep but stronger during non-REM sleep among deep-layer excitatory neurons. A subset of deep-layer neurons was active exclusively in the DOWN state of non-REM sleep. These results bridge mesoscopic LFPs and single-neuron interactions with laminar structure in V1.

KW - alpha rhythm

KW - cell types

KW - cortical layers

KW - current source density

KW - laminar recordings

KW - optogenetics

KW - oscillations

KW - primary visual cortex

KW - sleep

UR - http://www.scopus.com/inward/record.url?scp=85060343777&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85060343777&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2018.12.009

DO - 10.1016/j.neuron.2018.12.009

M3 - Article

C2 - 30635232

AN - SCOPUS:85060343777

SN - 0896-6273

VL - 101

SP - 500-513.e5

JO - Neuron

JF - Neuron

IS - 3

ER -

Layer-Specific Physiological Features and Interlaminar Interactions in the Primary Visual Cortex of the Mouse

Abstract

Funding

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this