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

Summary 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.

[1]  Sylvain Crochet,et al.  Synaptic Computation and Sensory Processing in Neocortical Layer 2/3 , 2013, Neuron.

[2]  G. Buzsáki,et al.  Pyramidal Cell-Interneuron Circuit Architecture and Dynamics in Hippocampal Networks , 2017, Neuron.

[3]  S. Hestrin,et al.  Correlation of Synaptic Inputs in the Visual Cortex of Awake, Behaving Mice , 2018, Neuron.

[4]  C. Schroeder,et al.  Neuronal Mechanisms of Cortical Alpha Oscillations in Awake-Behaving Macaques , 2008, The Journal of Neuroscience.

[5]  S. Hughes,et al.  The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators , 2010, Nature Neuroscience.

[6]  J. Alonso,et al.  Functional connectivity between simple cells and complex cells in cat striate cortex , 1998, Nature Neuroscience.

[7]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[8]  S. Hestrin,et al.  Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons , 2001, Science.

[9]  D. Leopold,et al.  Ongoing Alpha Activity in V1 Regulates Visually Driven Spiking Responses , 2017, Cerebral cortex.

[10]  Harvey A Swadlow,et al.  Stability of Thalamocortical Synaptic Transmission across Awake Brain States , 2009, The Journal of Neuroscience.

[11]  Y. Dan,et al.  Layer-specific network oscillation and spatiotemporal receptive field in the visual cortex , 2009, Proceedings of the National Academy of Sciences.

[12]  G. Buzsáki,et al.  Noradrenergic Control of Thalamic Oscillation: the Role of alpha-2 Receptors. , 1991, The European journal of neuroscience.

[13]  E. Callaway Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

[14]  D. McCormick,et al.  Sleep and arousal: thalamocortical mechanisms. , 1997, Annual review of neuroscience.

[15]  Arthur W. Wetzel,et al.  Network anatomy and in vivo physiology of visual cortical neurons , 2011, Nature.

[16]  B. Connors,et al.  Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. , 1991, Science.

[17]  U. Mitzdorf Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. , 1987, The International journal of neuroscience.

[18]  K. Harris,et al.  Laminar Structure of Spontaneous and Sensory-Evoked Population Activity in Auditory Cortex , 2009, Neuron.

[19]  Jyh-Jang Sun,et al.  Laminar and Columnar Structure of Sensory-Evoked Multineuronal Spike Sequences in Adult Rat Barrel Cortex In Vivo. , 2015, Cerebral cortex.

[20]  C. Torrence,et al.  A Practical Guide to Wavelet Analysis. , 1998 .

[21]  Eran Stark,et al.  Unbiased estimation of precise temporal correlations between spike trains , 2009, Journal of Neuroscience Methods.

[22]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[23]  Michael J. Goard,et al.  Fast Modulation of Visual Perception by Basal Forebrain Cholinergic Neurons , 2013, Nature Neuroscience.

[24]  J. Rinzel,et al.  Excitable dynamics of NREM sleep: a unifying model for neocortex and hippocampus , 2018, bioRxiv.

[25]  S. Hughes,et al.  Temporal Framing of Thalamic Relay-Mode Firing by Phasic Inhibition during the Alpha Rhythm , 2009, Neuron.

[26]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[27]  Kenneth D. Harris,et al.  Laminar-dependent effects of cortical state on auditory cortical spontaneous activity , 2012, Front. Neural Circuits.

[28]  P. Golshani,et al.  Visually Evoked 3–5 Hz Membrane Potential Oscillations Reduce the Responsiveness of Visual Cortex Neurons in Awake Behaving Mice , 2017, The Journal of Neuroscience.

[29]  Daniel Levenstein,et al.  Network Homeostasis and State Dynamics of Neocortical Sleep , 2016, Neuron.

[30]  Alexander S. Ecker,et al.  Principles of connectivity among morphologically defined cell types in adult neocortex , 2015, Science.

[31]  Christof Koch,et al.  Theta Phase Segregation of Input-Specific Gamma Patterns in Entorhinal-Hippocampal Networks , 2014, Neuron.

[32]  G. Buzsáki,et al.  Entorhinal-CA3 Dual-Input Control of Spike Timing in the Hippocampus by Theta-Gamma Coupling , 2017, Neuron.

[33]  Adriano B. L. Tort,et al.  Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task , 2008, Proceedings of the National Academy of Sciences.

[34]  Maria V. Sanchez-Vives,et al.  Cellular and network mechanisms of rhythmic recurrent activity in neocortex , 2000, Nature Neuroscience.

[35]  C. Gilbert,et al.  Top-down influences on visual processing , 2013, Nature Reviews Neuroscience.

[36]  M. Scanziani,et al.  Instantaneous Modulation of Gamma Oscillation Frequency by Balancing Excitation with Inhibition , 2009, Neuron.

[37]  Pierre Comon,et al.  Independent component analysis, A new concept? , 1994, Signal Process..

[38]  G. Buzsáki,et al.  Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. , 2004, Journal of neurophysiology.

[39]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[40]  György Buzsáki,et al.  Physiological Properties and Behavioral Correlates of Hippocampal Granule Cells and Mossy Cells , 2017, Neuron.

[41]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[42]  Brian R. Lee,et al.  Classification of electrophysiological and morphological types in mouse visual cortex , 2018, bioRxiv.

[43]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[44]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[45]  T. Branco,et al.  The probability of neurotransmitter release: variability and feedback control at single synapses , 2009, Nature Reviews Neuroscience.

[46]  C. Schroeder,et al.  A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. , 1998, Cerebral cortex.

[47]  F. Horvath,et al.  Electroencephalogram Rhythms correlated with Milk Reinforcement in Cats , 1964, Nature.

[48]  Eran Stark,et al.  Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. , 2012, Journal of neurophysiology.

[49]  Chun-I Yeh,et al.  Laminar analysis of visually evoked activity in the primary visual cortex , 2012, Proceedings of the National Academy of Sciences.

[50]  Takeshi Sakurai,et al.  Identification of a population of sleep-active cerebral cortex neurons , 2008, Proceedings of the National Academy of Sciences.

[51]  Valter Tucci,et al.  Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex , 2013, Nature Neuroscience.

[52]  L. Pickenhain,et al.  Hippocampal slow wave activity as a correlate of basic behavioral mechanisms in the rat. , 1967, Progress in brain research.

[53]  Eran Stark,et al.  Large-scale, high-density (up to 512 channels) recording of local circuits in behaving animals. , 2014, Journal of neurophysiology.

[54]  David A. Leopold,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[55]  D. R. Muir,et al.  Functional organization of excitatory synaptic strength in primary visual cortex , 2015, Nature.

[56]  W. M. Keck,et al.  Highly Selective Receptive Fields in Mouse Visual Cortex , 2008, The Journal of Neuroscience.

[57]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[58]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.

[59]  G. Shepherd,et al.  The neocortical circuit: themes and variations , 2015, Nature Neuroscience.

[60]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[61]  Kenneth D. Harris,et al.  Fast and accurate spike sorting of high-channel count probes with KiloSort , 2016, NIPS.

[62]  György Buzsáki,et al.  Noradrenergic Control of Thalamic Oscillation: the Role of α‐2 Receptors , 1991 .

[63]  O. Jensen,et al.  Gamma Power Is Phase-Locked to Posterior Alpha Activity , 2008, PloS one.

[64]  Long-Term Recordings Improve the Detection of Weak Excitatory–Excitatory Connections in Rat Prefrontal Cortex , 2014, The Journal of Neuroscience.

[65]  M. Carandini,et al.  Inhibition dominates sensory responses in awake cortex , 2012, Nature.

[66]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[67]  C. Schroeder,et al.  Neuronal Mechanisms and Attentional Modulation of Corticothalamic Alpha Oscillations , 2011, The Journal of Neuroscience.

[68]  Oscar Herreras,et al.  Schaffer-Specific Local Field Potentials Reflect Discrete Excitatory Events at Gamma Frequency That May Fire Postsynaptic Hippocampal CA1 Units , 2012, The Journal of Neuroscience.

[69]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[70]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.