Homeostatic control of neural activity: from phenomenology to molecular design.

Homeostasis is a specialized form of regulation that precisely maintains the function of a system at a set point level of activity. Recently, homeostatic signaling has been suggested to control neural activity through the modulation of synaptic efficacy and membrane excitability ( Davis & Goodman 1998a, Turrigiano & Nelson 2000, Marder & Prinz 2002, Perez-Otano & Ehlers 2005 ). In this way, homeostatic signaling is thought to constrain neural plasticity and contribute to the stability of neural function over time. Using a restrictive definition of homeostasis, this review first evaluates the phenomenological and molecular evidence for homeostatic signaling in the nervous system. Then, basic principles underlying the design and molecular implementation of homeostatic signaling are reviewed on the basis of work in other, simplified biological systems such as bacterial chemotaxis and the heat shock response. Data from these systems are then discussed in the context of homeostatic signaling in the nervous system.

[1]  A. Lupas,et al.  Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis. , 1989, The Journal of biological chemistry.

[2]  C. Gross,et al.  DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. , 1990, Genes & development.

[3]  E. Marder,et al.  Activity-dependent changes in the intrinsic properties of cultured neurons. , 1994, Science.

[4]  C. Goodman,et al.  Genetic Analysis of Glutamate Receptors in Drosophila Reveals a Retrograde Signal Regulating Presynaptic Transmitter Release , 1997, Neuron.

[5]  S. Leibler,et al.  Robustness in simple biochemical networks , 1997, Nature.

[6]  G. Fischbach,et al.  Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. , 1997, Science.

[7]  S. Chervitz,et al.  The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. , 1997, Annual review of cell and developmental biology.

[8]  E. Marder,et al.  A Model Neuron with Activity-Dependent Conductances Regulated by Multiple Calcium Sensors , 1998, The Journal of Neuroscience.

[9]  Aaron DiAntonio,et al.  Postsynaptic PKA Controls Quantal Size and Reveals a Retrograde Signal that Regulates Presynaptic Transmitter Release in Drosophila , 1998, Neuron.

[10]  C. Goodman,et al.  Genetic analysis of synaptic development and plasticity: homeostatic regulation of synaptic efficacy , 1998, Current Opinion in Neurobiology.

[11]  C. Goodman,et al.  Synapse-specific control of synaptic efficacy at the terminals of a single neuron , 1998, Nature.

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

[13]  E. Marder,et al.  Activity-Dependent Regulation of Potassium Currents in an Identified Neuron of the Stomatogastric Ganglion of the Crab Cancer borealis , 1999, The Journal of Neuroscience.

[14]  Niraj S. Desai,et al.  Plasticity in the intrinsic excitability of cortical pyramidal neurons , 1999, Nature Neuroscience.

[15]  Chris I. De Zeeuw,et al.  GATA-3 Is Involved in the Development of Serotonergic Neurons in the Caudal Raphe Nuclei , 1999, The Journal of Neuroscience.

[16]  U. Alon,et al.  Robustness in bacterial chemotaxis , 2022 .

[17]  C. Goodman,et al.  Glutamate Receptor Expression Regulates Quantal Size and Quantal Content at the Drosophila Neuromuscular Junction , 1999, The Journal of Neuroscience.

[18]  Niraj S. Desai,et al.  BDNF regulates the intrinsic excitability of cortical neurons. , 1999, Learning & memory.

[19]  Y. Kyōgoku,et al.  Translational induction of heat shock transcription factor sigma32: evidence for a built-in RNA thermosensor. , 1999, Genes & development.

[20]  M. V. Rossum,et al.  Activity Coregulates Quantal AMPA and NMDA Currents at Neocortical Synapses , 2000, Neuron.

[21]  S. Nelson,et al.  Hebb and homeostasis in neuronal plasticity , 2000, Current Opinion in Neurobiology.

[22]  J. Doyle,et al.  Robust perfect adaptation in bacterial chemotaxis through integral feedback control. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  T. Schikorski,et al.  Inactivity Produces Increases in Neurotransmitter Release and Synapse Size , 2001, Neuron.

[24]  G. Davis,et al.  Maintaining the stability of neural function: a homeostatic hypothesis. , 2001, Annual review of physiology.

[25]  E. Marder,et al.  Global Structure, Robustness, and Modulation of Neuronal Models , 2001, The Journal of Neuroscience.

[26]  Sacha B. Nelson,et al.  Postsynaptic Depolarization Scales Quantal Amplitude in Cortical Pyramidal Neurons , 2001, The Journal of Neuroscience.

[27]  A. Smit,et al.  Synapse Formation between Central Neurons Requires Postsynaptic Expression of the MEN1 Tumor Suppressor Gene , 2001, The Journal of Neuroscience.

[28]  G. Davis,et al.  Homeostatic Control of Presynaptic Release Is Triggered by Postsynaptic Membrane Depolarization , 2001, Neuron.

[29]  Wade Morishita,et al.  Control of Synaptic Strength by Glial TNFα , 2002, Science.

[30]  R. Malenka,et al.  Control of synaptic strength by glial TNFalpha. , 2002, Science.

[31]  Mark C. W. van Rossum,et al.  Activity Deprivation Reduces Miniature IPSC Amplitude by Decreasing the Number of Postsynaptic GABAA Receptors Clustered at Neocortical Synapses , 2002, The Journal of Neuroscience.

[32]  Richard D. Fetter,et al.  wishful thinking Encodes a BMP Type II Receptor that Regulates Synaptic Growth in Drosophila , 2002, Neuron.

[33]  R. Tsien,et al.  alpha- and betaCaMKII. Inverse regulation by neuronal activity and opposing effects on synaptic strength. , 2002, Neuron.

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

[35]  V. Murthy,et al.  Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons , 2002, Nature.

[36]  E. Marder,et al.  Failure of averaging in the construction of a conductance-based neuron model. , 2002, Journal of neurophysiology.

[37]  R. Tsien,et al.  α- and βCaMKII Inverse Regulation by Neuronal Activity and Opposing Effects on Synaptic Strength , 2002, Neuron.

[38]  M. Khammash,et al.  Calcium homeostasis and parturient hypocalcemia: an integral feedback perspective. , 2002, Journal of theoretical biology.

[39]  Eve Marder,et al.  Modeling stability in neuron and network function: the role of activity in homeostasis. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[40]  E. Marder,et al.  Episodic bouts of activity accompany recovery of rhythmic output by a neuromodulator- and activity-deprived adult neural network. , 2003, Journal of neurophysiology.

[41]  Reinhart Heinrich,et al.  The Roles of APC and Axin Derived from Experimental and Theoretical Analysis of the Wnt Pathway , 2003, PLoS biology.

[42]  C. Goodman,et al.  The BMP Homolog Gbb Provides a Retrograde Signal that Regulates Synaptic Growth at the Drosophila Neuromuscular Junction , 2003, Neuron.

[43]  Eve Marder,et al.  Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. , 2003, Journal of neurophysiology.

[44]  M. Ehlers,et al.  Activity-Dependent mRNA Splicing Controls ER Export and Synaptic Delivery of NMDA Receptors , 2003, Neuron.

[45]  An ER export signal accelerates the surface expression of shal potassium channels in pyloric neurons of the lobster stomatogastric ganglion , 2003, Pflügers Archiv.

[46]  V. Murthy,et al.  Synaptic gain control and homeostasis , 2003, Current Opinion in Neurobiology.

[47]  R. Nicoll,et al.  AMPA Receptor Trafficking at Excitatory Synapses , 2003, Neuron.

[48]  Eve Marder,et al.  Current Compensation in Neuronal Homeostasis , 2003, Neuron.

[49]  C. Goodman,et al.  Retrograde Control of Synaptic Transmission by Postsynaptic CaMKII at the Drosophila Neuromuscular Junction , 2003, Neuron.

[50]  Bruce R. Johnson,et al.  Activity-Independent Homeostasis in Rhythmically Active Neurons , 2003, Neuron.

[51]  E. Marder,et al.  Similar network activity from disparate circuit parameters , 2004, Nature Neuroscience.

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

[53]  Kevin G. Moffat,et al.  Article Title: Regulation of Neuronal Excitability through Pumilio- Dependent Control of a Sodium Channel Gene Regulation of Neuronal Excitability through Pumilio- Dependent Control of a Sodium Channel Gene Materials and Methods , 2022 .

[54]  Nicholas C. Spitzer,et al.  Activity-dependent homeostatic specification of transmitter expression in embryonic neurons , 2004, Nature.

[55]  J. Kaplan,et al.  Clathrin-mediated endocytosis is required for compensatory regulation of GLR-1 glutamate receptors after activity blockade. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[56]  S. Nelson,et al.  Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation , 2004, Nature Neuroscience.

[57]  Naama Barkai,et al.  Elucidating mechanisms underlying robustness of morphogen gradients. , 2004, Current opinion in genetics & development.

[58]  T. Horvath,et al.  CPG2 A brain- and synapse-specific protein that regulates the endocytosis of glutamate receptors , 2004, Neuron.

[59]  D. Eide,et al.  Eukaryotic zinc transporters and their regulation , 2001, Biometals.

[60]  G. Davis,et al.  Coordinating Structural and Functional Synapse Development: Postsynaptic p21-Activated Kinase Independently Specifies Glutamate Receptor Abundance and Postsynaptic Morphology , 2004, The Journal of Neuroscience.

[61]  Lindsey L. Glickfeld,et al.  Presynaptic homeostasis at CNS nerve terminals compensates for lack of a key Ca2+ entry pathway. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Aaron DiAntonio,et al.  Increased Expression of the Drosophila Vesicular Glutamate Transporter Leads to Excess Glutamate Release and a Compensatory Decrease in Quantal Content , 2004, The Journal of Neuroscience.

[63]  J. Stelling,et al.  Robustness of Cellular Functions , 2004, Cell.

[64]  G. Collingridge,et al.  Hippocalcin Functions as a Calcium Sensor in Hippocampal LTD , 2005, Neuron.

[65]  G. Davis,et al.  LIM Kinase1 Controls Synaptic Stability Downstream of the Type II BMP Receptor , 2005, Neuron.

[66]  Wade Morishita,et al.  Distinct triggering and expression mechanisms underlie LTD of AMPA and NMDA synaptic responses , 2005, Nature Neuroscience.

[67]  H. Adesnik,et al.  Stargazin modulates AMPA receptor gating and trafficking by distinct domains , 2005, Nature.

[68]  Stefan R. Pulver,et al.  Constant amplitude of postsynaptic responses for single presynaptic action potentials but not bursting input during growth of an identified neuromuscular junction in the lobster, Homarus americanus. , 2005, Journal of neurobiology.

[69]  R. Baines,et al.  Neuronal homeostasis through translational control , 2005, Molecular Neurobiology.

[70]  Rafael Yuste,et al.  Space matters: local and global dendritic Ca2+ compartmentalization in cortical interneurons , 2005, Trends in Neurosciences.

[71]  Michael D. Ehlers,et al.  Homeostatic plasticity and NMDA receptor trafficking , 2005, Trends in Neurosciences.

[72]  James E. Ferrell,et al.  Systems-Level Dissection of the Cell-Cycle Oscillator: Bypassing Positive Feedback Produces Damped Oscillations , 2005, Cell.

[73]  R. Huganir,et al.  Calcium-Permeable AMPA Receptor Plasticity Is Mediated by Subunit-Specific Interactions with PICK1 and NSF , 2005, Neuron.

[74]  John C. Doyle,et al.  Surviving heat shock: control strategies for robustness and performance. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Xiao-Jing Wang,et al.  The Stability of a Stochastic CaMKII Switch: Dependence on the Number of Enzyme Molecules and Protein Turnover , 2005, PLoS biology.

[76]  V. Pawlak,et al.  Impaired synaptic scaling in mouse hippocampal neurones expressing NMDA receptors with reduced calcium permeability , 2005, The Journal of physiology.

[77]  Eve Marder,et al.  Animal-to-Animal Variability in Motor Pattern Production in Adults and during Growth , 2005, The Journal of Neuroscience.

[78]  J. Isaacson,et al.  Synapse-Specific Downregulation of NMDA Receptors by Early Experience: A Critical Period for Plasticity of Sensory Input to Olfactory Cortex , 2005, Neuron.

[79]  R. Malenka,et al.  Differential Regulation of AMPA Receptor and GABA Receptor Trafficking by Tumor Necrosis Factor-α , 2005, The Journal of Neuroscience.

[80]  R. Tsien,et al.  Adaptation to Synaptic Inactivity in Hippocampal Neurons , 2005, Neuron.

[81]  John Guckenheimer,et al.  Activity-independent coregulation of IA and Ih in rhythmically active neurons. , 2005, Journal of neurophysiology.

[82]  Michael Wong,et al.  Advances in the pathophysiology of developmental epilepsies. , 2005, Seminars in pediatric neurology.

[83]  J. Gallant,et al.  Complete functional characterization of sensory neurons by system identification. , 2006, Annual review of neuroscience.

[84]  S. Hyman,et al.  Neural mechanisms of addiction: the role of reward-related learning and memory. , 2006, Annual review of neuroscience.

[85]  S. Cannon.  Pathomechanisms in channelopathies of skeletal muscle and brain. , 2006, Annual review of neuroscience.

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