Neuronal Firing Rate Homeostasis Is Inhibited by Sleep and Promoted by Wake

Homeostatic mechanisms stabilize neural circuit function by keeping firing rates within a set-point range, but whether this process is gated by brain state is unknown. Here, we monitored firing rate homeostasis in individual visual cortical neurons in freely behaving rats as they cycled between sleep and wake states. When neuronal firing rates were perturbed by visual deprivation, they gradually returned to a precise, cell-autonomous set point during periods of active wake, with lengthening of the wake period enhancing firing rate rebound. Unexpectedly, this resetting of neuronal firing was suppressed during sleep. This raises the possibility that memory consolidation or other sleep-dependent processes are vulnerable to interference from homeostatic plasticity mechanisms. PAPERCLIP.

[1]  Gordon X. Wang,et al.  Synaptic plasticity in sleep: learning, homeostasis and disease , 2011, Trends in Neurosciences.

[2]  G. Tononi,et al.  Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration , 2014, Neuron.

[3]  G. Tononi,et al.  Extensive and Divergent Effects of Sleep and Wakefulness on Brain Gene Expression , 2004, Neuron.

[4]  W. Gerstner,et al.  Connectivity reflects coding: a model of voltage-based STDP with homeostasis , 2010, Nature Neuroscience.

[5]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[6]  T. Hromádka,et al.  Sparse Representation of Sounds in the Unanesthetized Auditory Cortex , 2008, PLoS biology.

[7]  Kenji Mizuseki,et al.  Comparison of Sleep Spindles and Theta Oscillations in the Hippocampus , 2014, The Journal of Neuroscience.

[8]  V. Murthy,et al.  Synaptic plasticity: Rush hour traffic in the AMPA lanes , 2001, Current Biology.

[9]  M. Wilson,et al.  Optogenetic activation of cholinergic neurons in the PPT or LDT induces REM sleep , 2014, Proceedings of the National Academy of Sciences.

[10]  D. Hansel,et al.  On the Distribution of Firing Rates in Networks of Cortical Neurons , 2011, The Journal of Neuroscience.

[11]  Jadin C. Jackson,et al.  Quantitative measures of cluster quality for use in extracellular recordings , 2005, Neuroscience.

[12]  Anubhuthi Goel,et al.  Persistence of Experience-Induced Homeostatic Synaptic Plasticity through Adulthood in Superficial Layers of Mouse Visual Cortex , 2007, The Journal of Neuroscience.

[13]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[14]  R. Malenka,et al.  Synaptic scaling mediated by glial TNF-alpha. , 2006, Nature.

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

[16]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[17]  G. Tononi,et al.  Lempel-Ziv complexity of cortical activity during sleep and waking in rats , 2015, Journal of neurophysiology.

[18]  R. Reid,et al.  Homeostatic Regulation of Eye-Specific Responses in Visual Cortex during Ocular Dominance Plasticity , 2007, Neuron.

[19]  M. Bear,et al.  Bidirectional synaptic mechanisms of ocular dominance plasticity in visual cortex , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  M. Weliky,et al.  Small modulation of ongoing cortical dynamics by sensory input during natural vision , 2004, Nature.

[21]  R. Malenka,et al.  Synaptic scaling mediated by glial TNF-α , 2006, Nature.

[22]  Steven W. Flavell,et al.  Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. , 2008, Annual review of neuroscience.

[23]  Sara J. Aton,et al.  Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons , 2013, Proceedings of the National Academy of Sciences.

[24]  G. Tononi,et al.  Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep , 2008, Nature Neuroscience.

[25]  Peter Meerlo,et al.  New neurons in the adult brain: the role of sleep and consequences of sleep loss. , 2009, Sleep medicine reviews.

[26]  Aneesha K. Suresh,et al.  Sleep promotes cortical response potentiation following visual experience. , 2014, Sleep.

[27]  Bruno Rossion,et al.  Figures and figure supplements , 2014 .

[28]  G. Turrigiano,et al.  Rapid Synaptic Scaling Induced by Changes in Postsynaptic Firing , 2008, Neuron.

[29]  G. Turrigiano,et al.  Synaptic Scaling Requires the GluR2 Subunit of the AMPA Receptor , 2009, The Journal of Neuroscience.

[30]  M. Carandini,et al.  Cortical State Determines Global Variability and Correlations in Visual Cortex , 2015, The Journal of Neuroscience.

[31]  B. Jones,et al.  From waking to sleeping: neuronal and chemical substrates. , 2005, Trends in pharmacological sciences.

[32]  Keith B. Hengen,et al.  Firing Rate Homeostasis in Visual Cortex of Freely Behaving Rodents , 2013, Neuron.

[33]  M. Steriade,et al.  Neuronal Plasticity in Thalamocortical Networks during Sleep and Waking Oscillations , 2003, Neuron.

[34]  Gina G. Turrigiano,et al.  Tumor Necrosis Factor-α Signaling Maintains the Ability of Cortical Synapses to Express Synaptic Scaling , 2010, The Journal of Neuroscience.

[35]  R. Lydic,et al.  M2 muscarinic receptors in pontine reticular formation of C57BL/6J mouse contribute to rapid eye movement sleep generation , 2004, Neuroscience.

[36]  S. Nelson,et al.  Strength through Diversity , 2008, Neuron.

[37]  G. Turrigiano Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. , 2012, Cold Spring Harbor perspectives in biology.

[38]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[39]  Georg B. Keller,et al.  Synaptic Scaling and Homeostatic Plasticity in the Mouse Visual Cortex In Vivo , 2013, Neuron.

[40]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[41]  A. Lüthi,et al.  Insufficient Sleep Reversibly Alters Bidirectional Synaptic Plasticity and NMDA Receptor Function , 2006, The Journal of Neuroscience.

[42]  I. Nelken,et al.  Interplay between population firing stability and single neuron dynamics in hippocampal networks , 2015, eLife.

[43]  G. Tononi,et al.  Cortical Firing and Sleep Homeostasis , 2009, Neuron.

[44]  M. Walker,et al.  Sleep, Plasticity and Memory from Molecules to Whole-Brain Networks , 2013, Current Biology.

[45]  M. Mirmiran,et al.  Effect of light intensity on diurnal sleep-wake distribution in young and old rats , 1993, Brain Research Bulletin.

[46]  Jessica A. Cardin,et al.  Stimulus Feature Selectivity in Excitatory and Inhibitory Neurons in Primary Visual Cortex , 2007, The Journal of Neuroscience.

[47]  M. Bear,et al.  NMDA Receptor-Dependent Ocular Dominance Plasticity in Adult Visual Cortex , 2003, Neuron.

[48]  Niraj S. Desai,et al.  Critical periods for experience-dependent synaptic scaling in visual cortex , 2002, Nature Neuroscience.

[49]  K. Miller,et al.  Modeling the Dynamic Interaction of Hebbian and Homeostatic Plasticity , 2014, Neuron.

[50]  K. Svoboda,et al.  Neural Activity in Barrel Cortex Underlying Vibrissa-Based Object Localization in Mice , 2010, Neuron.

[51]  Gina G. Turrigiano,et al.  Multiple Modes of Network Homeostasis in Visual Cortical Layer 2/3 , 2008, The Journal of Neuroscience.

[52]  Daniel J. R. Christensen,et al.  Sleep Drives Metabolite Clearance from the Adult Brain , 2013, Science.

[53]  Alain Destexhe,et al.  Inhibition Determines Membrane Potential Dynamics and Controls Action Potential Generation in Awake and Sleeping Cat Cortex , 2007, The Journal of Neuroscience.

[54]  G. Buzsáki,et al.  REM Sleep Reorganizes Hippocampal Excitability , 2012, Neuron.

[55]  G. Bertini,et al.  Experimental sleep deprivation as a tool to test memory deficits in rodents , 2013, Front. Syst. Neurosci..

[56]  Michael P. Stryker,et al.  Report Tumor Necrosis Factor-a Mediates One Component of Competitive, Experience-dependent Plasticity in Developing Visual Cortex , 2022 .

[57]  Nicholas A. Steinmetz,et al.  Mechanisms of Sleep-Dependent Consolidation of Cortical Plasticity , 2009, Neuron.

[58]  Randy M. Bruno,et al.  Effects and Mechanisms of Wakefulness on Local Cortical Networks , 2011, Neuron.

[59]  Y. Goda,et al.  The interplay between Hebbian and homeostatic synaptic plasticity , 2013, The Journal of cell biology.

[60]  E. Evarts,et al.  Spontaneous Discharge of Single Neurons during Sleep and Waking , 1962, Science.

[61]  M. Stryker,et al.  Sleep Enhances Plasticity in the Developing Visual Cortex , 2001, Neuron.

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

[63]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[64]  M. Frank,et al.  Sleep, clocks, and synaptic plasticity , 2014, Trends in Neurosciences.

[65]  G. Tononi,et al.  Direct Evidence for Wake-Related Increases and Sleep-Related Decreases in Synaptic Strength in Rodent Cortex , 2010, The Journal of Neuroscience.

[66]  G. Turrigiano,et al.  Synaptic and Intrinsic Homeostatic Mechanisms Cooperate to Increase L2/3 Pyramidal Neuron Excitability during a Late Phase of Critical Period Plasticity , 2013, The Journal of Neuroscience.

[67]  R. Nicoll,et al.  Single-Cell Optogenetic Excitation Drives Homeostatic Synaptic Depression , 2010, Neuron.