The dependence of neuronal encoding efficiency on Hebbian plasticity and homeostatic regulation of neurotransmitter release

Synapses act as information filters by different molecular mechanisms including retrograde messenger that affect neuronal spiking activity. One of the well-known effects of retrograde messenger in presynaptic neurons is a change of the probability of neurotransmitter release. Hebbian learning describe a strengthening of a synapse between a presynaptic input onto a postsynaptic neuron when both pre- and postsynaptic neurons are coactive. In this work, a theory of homeostatic regulation of neurotransmitter release by retrograde messenger and Hebbian plasticity in neuronal encoding is presented. Encoding efficiency was measured for different synaptic conditions. In order to gain high encoding efficiency, the spiking pattern of a neuron should be dependent on the intensity of the input and show low levels of noise. In this work, we represent spiking trains as zeros and ones (corresponding to non-spike or spike in a time bin, respectively) as words with length equal to three. Then the frequency of each word (here eight words) is measured using spiking trains. These frequencies are used to measure neuronal efficiency in different conditions and for different parameter values. Results show that neurons that have synapses acting as band-pass filters show the highest efficiency to encode their input when both Hebbian mechanism and homeostatic regulation of neurotransmitter release exist in synapses. Specifically, the integration of homeostatic regulation of feedback inhibition with Hebbian mechanism and homeostatic regulation of neurotransmitter release in the synapses leads to even higher efficiency when high stimulus intensity is presented to the neurons. However, neurons with synapses acting as high-pass filters show no remarkable increase in encoding efficiency for all simulated synaptic plasticity mechanisms. This study demonstrates the importance of cooperation of Hebbian mechanism with regulation of neurotransmitter release induced by rapid diffused retrograde messenger in neurons with synapses as low and band-pass filters to obtain high encoding efficiency in different environmental and physiological conditions.

[1]  Chung-Chuan Lo,et al.  Top-Down Modulation on Perceptual Decision with Balanced Inhibition through Feedforward and Feedback Inhibitory Neurons , 2013, PloS one.

[2]  Joshua Tate Dudman,et al.  The inhibitory microcircuit of the substantia nigra provides feedback gain control of the basal ganglia output , 2014, eLife.

[3]  R. Malenka,et al.  Synaptic Plasticity: Multiple Forms, Functions, and Mechanisms , 2008, Neuropsychopharmacology.

[4]  Rick Quax,et al.  Applying Information Theory to Neuronal Networks: From Theory to Experiments , 2014, Entropy.

[5]  G. Davis.  Homeostatic Signaling and the Stabilization of Neural Function , 2013, Neuron.

[6]  Zev Balsen,et al.  Sensory Neuron Signaling to the Brain: Properties of Transmitter Release from Olfactory Nerve Terminals , 2004, The Journal of Neuroscience.

[7]  T. Südhof,et al.  Synaptotagmin I functions as a calcium regulator of release probability , 2001, Nature.

[8]  P. Dayan.  Twenty-Five Lessons from Computational Neuromodulation , 2012, Neuron.

[9]  P. Castillo,et al.  Endocannabinoid Signaling and Synaptic Function , 2012, Neuron.

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

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

[12]  T. Südhof,et al.  Calcium regulation of neurotransmitter release: reliably unreliable? , 1997, Current opinion in cell biology.

[13]  V. Kolb-Bachofen,et al.  The role of nitric oxide. , 2006, Rheumatology.

[14]  Y. Goda,et al.  Unraveling Mechanisms of Homeostatic Synaptic Plasticity , 2010, Neuron.

[15]  S. Grant.  Synaptopathies: diseases of the synaptome , 2012, Current Opinion in Neurobiology.

[16]  Jian-Guo Chen,et al.  The Physiology of BDNF and Its Relationship with ADHD , 2014, Molecular Neurobiology.

[17]  Dirk Bucher,et al.  Homeostatic Plasticity in the Nervous System , 2012, Neural plasticity.

[18]  Martin J. Schmidt,et al.  Inhibition of parvalbumin-expressing interneurons results in complex behavioral changes , 2014, Molecular Psychiatry.

[19]  Stephen Coombes,et al.  A Biophysical Model of Endocannabinoid-Mediated Short Term Depression in Hippocampal Inhibition , 2013, PloS one.

[20]  Charles F Stevens,et al.  Synaptic plasticity , 1998, Current Biology.

[21]  R. Tsien,et al.  Postsynaptic GluA1 enables acute retrograde enhancement of presynaptic function to coordinate adaptation to synaptic inactivity , 2010, Proceedings of the National Academy of Sciences.

[22]  M. Ehlers,et al.  Glutamate Receptor Dynamics in Dendritic Microdomains , 2008, Neuron.

[23]  M. Kano,et al.  Endocannabinoid-mediated retrograde modulation of synaptic transmission , 2014, Current Opinion in Neurobiology.

[24]  M. Kano,et al.  Endocannabinoids and Retrograde Modulation of Synaptic Transmission , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[26]  L. Weiss,et al.  Cell adhesion. , 1978, International dental journal.

[27]  R. Huganir,et al.  The cell biology of synaptic plasticity: AMPA receptor trafficking. , 2007, Annual review of cell and developmental biology.

[28]  D. A. Baxter,et al.  Current- and voltage-clamp recordings and computer simulations of Kenyon cells in the honeybee. , 2004, Journal of neurophysiology.

[29]  G D Lewen,et al.  Reproducibility and Variability in Neural Spike Trains , 1997, Science.

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

[31]  G. Turrigiano.  The Self-Tuning Neuron: Synaptic Scaling of Excitatory Synapses , 2008, Cell.

[32]  Synaptic plasticity: Timing is everything , 2014, Nature Reviews Neuroscience.

[33]  E. Marder.  Neuromodulation of Neuronal Circuits: Back to the Future , 2012, Neuron.

[34]  K. Miller,et al.  A Theory of the Transition to Critical Period Plasticity: Inhibition Selectively Suppresses Spontaneous Activity , 2013, Neuron.

[35]  W. Gerstner,et al.  Synaptic Consolidation: From Synapses to Behavioral Modeling , 2015, The Journal of Neuroscience.

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

[37]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[38]  S. Grant,et al.  Comparative Study of Human and Mouse Postsynaptic Proteomes Finds High Compositional Conservation and Abundance Differences for Key Synaptic Proteins , 2012, PloS one.

[39]  P. P. C. R. Karunasekara,et al.  Understanding Neural Population Coding: Information Theoretic Insights from the Auditory System , 2014 .

[40]  K. Fox,et al.  The role of nitric oxide in pre-synaptic plasticity and homeostasis , 2013, Front. Cell. Neurosci..

[41]  W. Regehr,et al.  Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. , 2014, Annual review of physiology.

[42]  F. Benfenati.  Synaptic plasticity and the neurobiology of learning and memory. , 2007, Acta bio-medica : Atenei Parmensis.

[43]  Kenji Doya,et al.  Introduction for 2002 Special Issue: Computational Models of Neuromodulation , 2002, Neural Networks.

[44]  T. Mittmann,et al.  NO regulates the strength of synaptic inputs onto hippocampal CA1 neurons via NO-GC1/cGMP signalling , 2014, Pflügers Archiv - European Journal of Physiology.

[45]  Romesh D Kumbhani,et al.  Precision, reliability, and information-theoretic analysis of visual thalamocortical neurons. , 2007, Journal of neurophysiology.

[46]  L. Abbott,et al.  Synaptic computation , 2004, Nature.

[47]  M. A. Sutton,et al.  Local Presynaptic Activity Gates Homeostatic Changes in Presynaptic Function Driven by Dendritic BDNF Synthesis , 2010, Neuron.

[48]  N. Emptage,et al.  Two sides to long-term potentiation: a view towards reconciliation , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[49]  György Buzsáki,et al.  Tasks for inhibitory interneurons in intact brain circuits , 2015, Neuropharmacology.

[50]  Y. Goda,et al.  Dendritic signalling and homeostatic adaptation , 2009, Current Opinion in Neurobiology.

[51]  D. Dickman,et al.  A Hierarchy of Cell Intrinsic and Target-Derived Homeostatic Signaling , 2010, Neuron.

[52]  B. Lu,et al.  BDNF and synaptic plasticity, cognitive function, and dysfunction. , 2014, Handbook of experimental pharmacology.

[53]  D. Qiu,et al.  Nitric oxide facilitates active avoidance learning via enhancement of glutamate levels in the hippocampal dentate gyrus , 2014, Behavioural Brain Research.

[54]  Donna J. Calu,et al.  Intrinsic plasticity: an emerging player in addiction , 2015, Nature Reviews Neuroscience.

[55]  R. Silver,et al.  High-Probability Uniquantal Transmission at Excitatory Synapses in Barrel Cortex , 2003, Science.

[56]  Florentin Wörgötter,et al.  Time scales of memory, learning, and plasticity , 2012, Biological Cybernetics.

[57]  E. Kavalali.  The mechanisms and functions of spontaneous neurotransmitter release , 2014, Nature Reviews Neuroscience.

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

[59]  J. Piek,et al.  Coupling online control and inhibitory systems in children with Developmental Coordination Disorder: Goal-directed reaching. , 2015, Research in developmental disabilities.

[60]  Jin Fan,et al.  An information theory account of cognitive control , 2014, Front. Hum. Neurosci..

[61]  G. Turrigiano.  Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. , 2011, Annual review of neuroscience.

[62]  Florentin Wörgötter,et al.  An information theoretic model of information processing in the Drosophila olfactory system: the role of inhibitory neurons for system efficiency , 2013, Front. Comput. Neurosci..

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

[64]  J. Molgó,et al.  Early Presynaptic and Postsynaptic Calcium Signaling Abnormalities Mask Underlying Synaptic Depression in Presymptomatic Alzheimer's Disease Mice , 2012, The Journal of Neuroscience.

[65]  P. Uhlhaas,et al.  Neural oscillations as a translational tool in schizophrenia research: Rationale, paradigms and challenges , 2015, Journal of psychopharmacology.

[66]  Kevin F. H. Lee,et al.  Tuning into diversity of homeostatic synaptic plasticity , 2014, Neuropharmacology.

[67]  Joseph E LeDoux,et al.  Structural plasticity and memory , 2004, Nature Reviews Neuroscience.

[68]  G. Davis,et al.  Homeostatic control of presynaptic neurotransmitter release. , 2015, Annual review of physiology.

[69]  K. Jezek,et al.  Developmental Refinement of Vesicle Cycling at Schaffer Collateral Synapses , 2013, Neuron.

[70]  E. Marder,et al.  Variability, compensation and homeostasis in neuron and network function , 2006, Nature Reviews Neuroscience.

[71]  Maria Andres-Alonso,et al.  Molecular mechanisms driving homeostatic plasticity of neurotransmitter release , 2013, Front. Cell. Neurosci..

[72]  Faramarz Faghihi,et al.  Impaired homeostatic regulation of feedback inhibition associated with system deficiency to detect fluctuation in stimulus intensity: a simulation study , 2015, Neurocomputing.

[73]  Anders Lansner,et al.  Synaptic and nonsynaptic plasticity approximating probabilistic inference , 2014, Front. Synaptic Neurosci..

[74]  Tomonori Takeuchi,et al.  The synaptic plasticity and memory hypothesis: encoding, storage and persistence , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[75]  W. Regehr,et al.  Variance-Mean Analysis in the Presence of a Rapid Antagonist Indicates Vesicle Depletion Underlies Depression at the Climbing Fiber Synapse , 2004, Neuron.

[76]  A. Hannan,et al.  Dysregulation of synaptic proteins, dendritic spine abnormalities and pathological plasticity of synapses as experience-dependent mediators of cognitive and psychiatric symptoms in Huntington’s disease , 2013, Neuroscience.

[77]  Dirk Bucher,et al.  Neuromodulation of neurons and synapses , 2014, Current Opinion in Neurobiology.

[78]  Quan Yuan,et al.  Structural homeostasis in the nervous system: a balancing act for wiring plasticity and stability , 2015, Front. Cell. Neurosci..

[79]  G. Davis.  Homeostatic control of neural activity: from phenomenology to molecular design. , 2006, Annual review of neuroscience.

[80]  P. Greengard,et al.  Nitric oxide regulates synaptic transmission between spiny projection neurons , 2014, Proceedings of the National Academy of Sciences.

[81]  Wulfram Gerstner,et al.  Synaptic Plasticity in Neural Networks Needs Homeostasis with a Fast Rate Detector , 2013, PLoS Comput. Biol..

[82]  Nicole Calakos,et al.  Presynaptic long-term plasticity , 2013, Front. Synaptic Neurosci..