Impacts of Spike Shape Variations on Synaptic Communication

Understanding the communication theoretical capabilities of information transmission among neurons, known as neuro-spike communication, is a significant step in developing bio-inspired solutions for nanonetworking. In this paper, we focus on a part of this communication known as synaptic transmission for pyramidal neurons in the Cornu Ammonis area of the hippocampus location in the brain and propose a communication-based model for it that includes effects of spike shape variation on neural calcium signaling and the vesicle release process downstream of it. For this aim, we find impacts of spike shape variation on opening of voltage-dependent calcium channels, which control the release of vesicles from the pre-synaptic neuron by changing the influx of calcium ions. Moreover, we derive the structure of the optimum receiver based on the Neyman–Pearson detection method to find the effects of spike shape variations on the functionality of neuro-spike communication. Numerical results depict that changes in both spike width and amplitude affect the error detection probability. Moreover, these two factors do not control the performance of the system independently. Hence, a proper model for neuro-spike communication should contain effects of spike shape variations during axonal transmission on both synaptic propagation and spike generation mechanisms to enable us to accurately explain the performance of this communication paradigm.

[1]  Ozgur B. Akan,et al.  A Communication Theoretical Modeling of Axonal Propagation in Hippocampal Pyramidal Neurons , 2017, IEEE Transactions on NanoBioscience.

[2]  Robert H. Chow,et al.  A two-step model of secretion control in neuroendocrine cells , 1993, Pflügers Archiv.

[3]  X. Wang,et al.  Implications of All-or-None Synaptic Transmission and Short-Term Depression beyond Vesicle Depletion: A Computational Study , 2000, The Journal of Neuroscience.

[4]  Robert Plonsey,et al.  Bioelectricity: A Quantitative Approach Duke University’s First MOOC , 2013 .

[5]  Nelson Spruston,et al.  Distance-Dependent Differences in Synapse Number and AMPA Receptor Expression in Hippocampal CA1 Pyramidal Neurons , 2006, Neuron.

[6]  W G Regehr,et al.  Control of Neurotransmitter Release by Presynaptic Waveform at the Granule Cell to Purkinje Cell Synapse , 1997, The Journal of Neuroscience.

[7]  Özgür B. Akan,et al.  Importance of vesicle release stochasticity in neuro-spike communication , 2017, 2017 39th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[8]  Michael B. Hoppa,et al.  Control and Plasticity of the Presynaptic Action Potential Waveform at Small CNS Nerve Terminals , 2014, Neuron.

[9]  C. Stevens,et al.  Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Özgür B. Akan,et al.  A Communication Theoretical Analysis of Synaptic Multiple-Access Channel in Hippocampal-Cortical Neurons , 2013, IEEE Transactions on Communications.

[11]  Barry W. Connors,et al.  Neuroscience: Exploring the brain, 3rd ed. , 2007 .

[12]  Laura Galluccio,et al.  Characterization of molecular communications among implantable biomedical neuro-inspired nanodevices , 2013, Nano Commun. Networks.

[13]  G. Shepherd,et al.  Three-Dimensional Structure and Composition of CA3→CA1 Axons in Rat Hippocampal Slices: Implications for Presynaptic Connectivity and Compartmentalization , 1998, The Journal of Neuroscience.

[14]  Laura Galluccio,et al.  Modeling signal propagation in nanomachine-to-neuron communications , 2011, Nano Commun. Networks.

[15]  D. Kullmann,et al.  Differential triggering of spontaneous glutamate release by P/Q-, N-, and R-type Ca2+ channels , 2013, Nature Neuroscience.

[16]  Ozgur B. Akan,et al.  Rate region analysis of multi-terminal neuronal nanoscale molecular communication channel , 2017, 2017 IEEE 17th International Conference on Nanotechnology (IEEE-NANO).

[17]  P. Jonas,et al.  Differential Gating and Recruitment of P/Q-, N-, and R-Type Ca2+ Channels in Hippocampal Mossy Fiber Boutons , 2007, The Journal of Neuroscience.

[18]  P. Jonas,et al.  Dynamic Control of Presynaptic Ca2+ Inflow by Fast-Inactivating K+ Channels in Hippocampal Mossy Fiber Boutons , 2000, Neuron.

[19]  D. Sulzer,et al.  Vesicles Equal in Neurotransmitter Concentration but Not in Volume , 2000, Neuron.

[20]  Özgür B. Akan,et al.  A Physical Channel Model for Nanoscale Neuro-Spike Communications , 2013, IEEE Transactions on Communications.

[21]  W. Betz,et al.  Synaptic vesicle pools , 2005, Nature Reviews Neuroscience.

[22]  T. Schikorski,et al.  Quantitative Ultrastructural Analysis of Hippocampal Excitatory Synapses Materials and Methods Terminology Fixation and Embedding , 2022 .

[23]  M. Fernandez,et al.  Closed-Form Expression for the Poisson-Binomial Probability Density Function , 2010, IEEE Transactions on Aerospace and Electronic Systems.

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

[25]  R. Tsien,et al.  Synaptic vesicle pools and dynamics. , 2012, Cold Spring Harbor perspectives in biology.

[26]  Ilangko Balasingham,et al.  From Nano-Scale Neural Excitability to Long Term Synaptic Modification , 2014, NANOCOM' 14.

[27]  K. Svoboda,et al.  The Number of Glutamate Receptors Opened by Synaptic Stimulation in Single Hippocampal Spines , 2004, The Journal of Neuroscience.

[28]  C. Stevens,et al.  Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses , 1997, Neuron.

[29]  J. Magee,et al.  Mechanism of the distance‐dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons , 2003, The Journal of physiology.

[30]  J. Bekkers,et al.  N- and P/Q-Type Ca2+ Channels Mediate Transmitter Release with a Similar Cooperativity at Rat Hippocampal Autapses , 1998, The Journal of Neuroscience.

[31]  Christof Koch,et al.  Detecting and Estimating Signals over Noisy and Unreliable Synapses: Information-Theoretic Analysis , 2001, Neural Computation.

[32]  P. Saggau,et al.  Modulation of transmitter release by action potential duration at the hippocampal CA3-CA1 synapse. , 1999, Journal of neurophysiology.

[33]  Özgür B. Akan,et al.  Synaptic Channel Model Including Effects of Spike Width Variation , 2015, NANOCOM.

[34]  Dominique M. Durand,et al.  High Frequency Stimulation Extends the Refractory Period and Generates Axonal Block in the Rat Hippocampus , 2014, Brain Stimulation.

[35]  J. Magee,et al.  Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons , 2000, Nature Neuroscience.

[36]  Murat Kuscu,et al.  Fundamentals of Molecular Information and Communication Science , 2017, Proceedings of the IEEE.