When Less Is More: Non-monotonic Spike Sequence Processing in Neurons

Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies on neuronal input-output relations have focused on continuous-time inputs such as constant or noisy sinusoidal currents. Yet, most neurons comm...

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Published inPLoS computational biology Vol. 11; no. 2; p. e1004002
Main Authors Arnoldt, Hinrich, Chang, Shuwen, Jahnke, Sven, Urmersbach, Birk, Taschenberger, Holger, Timme, Marc
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.02.2015
Public Library of Science (PLoS)
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ISSN1553-7358
1553-734X
1553-7358
DOI10.1371/journal.pcbi.1004002

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Abstract Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies on neuronal input-output relations have focused on continuous-time inputs such as constant or noisy sinusoidal currents. Yet, most neurons communicate via exchanging action potentials (spikes) at discrete times. Here, we systematically analyze the stationary spiking response to regular spiking inputs and reveal that it is generically non-monotonic. Our theoretical analysis shows that the underlying mechanism relies solely on a combination of the discrete nature of the communication by spikes, the capability of locking output to input spikes and limited resources required for spike processing. Numerical simulations of mathematically idealized and biophysically detailed models, as well as neurophysiological experiments confirm and illustrate our theoretical predictions.
AbstractList Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies on neuronal input-output relations have focused on continuous-time inputs such as constant or noisy sinusoidal currents. Yet, most neurons communicate via exchanging action potentials (spikes) at discrete times. Here, we systematically analyze the stationary spiking response to regular spiking inputs and reveal that it is generically non-monotonic. Our theoretical analysis shows that the underlying mechanism relies solely on a combination of the discrete nature of the communication by spikes, the capability of locking output to input spikes and limited resources required for spike processing. Numerical simulations of mathematically idealized and biophysically detailed models, as well as neurophysiological experiments confirm and illustrate our theoretical predictions.
Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies on neuronal input-output relations have focused on continuous-time inputs such as constant or noisy sinusoidal currents. Yet, most neurons communicate via exchanging action potentials (spikes) at discrete times. Here, we systematically analyze the stationary spiking response to regular spiking inputs and reveal that it is generically non-monotonic. Our theoretical analysis shows that the underlying mechanism relies solely on a combination of the discrete nature of the communication by spikes, the capability of locking output to input spikes and limited resources required for spike processing. Numerical simulations of mathematically idealized and biophysically detailed models, as well as neurophysiological experiments confirm and illustrate our theoretical predictions. Brain function relies on robust communication between a huge number of nerve cells (neurons) that exchange short-lasting electrical pulses (called action potentials or spikes) at certain times. How nerve cells process their spiking inputs to generate spiking outputs thus is key not only to individual neurons’ computational capabilities but also to the collective dynamics of neuronal networks. Here we analyze the response properties of neurons to regular spike sequence inputs. We find that neurons typically respond in a non-monotonic way. Output frequency mostly increases with input frequency as expected but sometimes output frequency necessarily decreases upon increasing the input frequency. Our theoretical analysis predicts that spiking neurons commonly exhibit such non-monotonic response properties. Simulations of simple mathematical and complex computational models as well as neurophysiological experiments confirm our theoretical predictions.
  Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies on neuronal input-output relations have focused on continuous-time inputs such as constant or noisy sinusoidal currents. Yet, most neurons communicate via exchanging action potentials (spikes) at discrete times. Here, we systematically analyze the stationary spiking response to regular spiking inputs and reveal that it is generically non-monotonic. Our theoretical analysis shows that the underlying mechanism relies solely on a combination of the discrete nature of the communication by spikes, the capability of locking output to input spikes and limited resources required for spike processing. Numerical simulations of mathematically idealized and biophysically detailed models, as well as neurophysiological experiments confirm and illustrate our theoretical predictions.
Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies on neuronal input-output relations have focused on continuous-time inputs such as constant or noisy sinusoidal currents. Yet, most neurons communicate via exchanging action potentials (spikes) at discrete times. Here, we systematically analyze the stationary spiking response to regular spiking inputs and reveal that it is generically non-monotonic. Our theoretical analysis shows that the underlying mechanism relies solely on a combination of the discrete nature of the communication by spikes, the capability of locking output to input spikes and limited resources required for spike processing. Numerical simulations of mathematically idealized and biophysically detailed models, as well as neurophysiological experiments confirm and illustrate our theoretical predictions.Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies on neuronal input-output relations have focused on continuous-time inputs such as constant or noisy sinusoidal currents. Yet, most neurons communicate via exchanging action potentials (spikes) at discrete times. Here, we systematically analyze the stationary spiking response to regular spiking inputs and reveal that it is generically non-monotonic. Our theoretical analysis shows that the underlying mechanism relies solely on a combination of the discrete nature of the communication by spikes, the capability of locking output to input spikes and limited resources required for spike processing. Numerical simulations of mathematically idealized and biophysically detailed models, as well as neurophysiological experiments confirm and illustrate our theoretical predictions.
Audience Academic
Author Arnoldt, Hinrich
Taschenberger, Holger
Chang, Shuwen
Urmersbach, Birk
Jahnke, Sven
Timme, Marc
AuthorAffiliation 3 Department of Membrane Biophysics, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
4 Bernstein Center for Computational Neuroscience (BCCN) Göttingen, Göttingen, Germany
1 Network Dynamics, Max Planck Institute for Dynamics and Self-Organization (MPIDS), Göttingen, Germany
2 Institute for Nonlinear Dynamics, Faculty of Physics, Georg August University Göttingen, Göttingen, Germany
Université Paris Descartes, Centre National de la Recherche Scientifique, FRANCE
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CitedBy_id crossref_primary_10_1098_rsif_2018_0408
crossref_primary_10_3389_fncel_2019_00456
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The authors have declared that no competing interests exist.
Conceived and designed the experiments: HA SC SJ BU HT MT. Performed the experiments: HA SC SJ BU. Analyzed the data: HA SC SJ BU HT MT. Contributed reagents/materials/analysis tools: HA SC SJ BU HT MT. Wrote the paper: HA HT MT. Developed the theory: HA MT.
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– reference: 26436417 - PLoS Comput Biol. 2015 Oct;11(10):e1004380
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Snippet Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies on...
  Fundamental response properties of neurons centrally underly the computational capabilities of both individual nerve cells and neural networks. Most studies...
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SubjectTerms Action Potentials - physiology
Animals
Cells, Cultured
Computer Simulation
Experiments
Models, Neurological
Neural circuitry
Neural networks
Neurons
Neurons - physiology
Numerical analysis
Patch-Clamp Techniques
Physiological aspects
Rats
Rats, Wistar
Software
Studies
Trapezoid Body - cytology
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Title When Less Is More: Non-monotonic Spike Sequence Processing in Neurons
URI https://www.ncbi.nlm.nih.gov/pubmed/25646860
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https://pubmed.ncbi.nlm.nih.gov/PMC4315492
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http://dx.doi.org/10.1371/journal.pcbi.1004002
Volume 11
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