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Title: Balanced Excitatory and Inhibitory Synaptic Currents Promote Efficient Coding and Metabolic Efficiency

Abstract

A balance between excitatory and inhibitory synaptic currents is thought to be important for several aspects of information processing in cortical neurons in vivo, including gain control, bandwidth and receptive field structure. These factors will affect the firing rate of cortical neurons and their reliability, with consequences for their information coding and energy consumption. Yet how balanced synaptic currents contribute to the coding efficiency and energy efficiency of cortical neurons remains unclear. We used single compartment computational models with stochastic voltage-gated ion channels to determine whether synaptic regimes that produce balanced excitatory and inhibitory currents have specific advantages over other input regimes. Specifically, we compared models with only excitatory synaptic inputs to those with equal excitatory and inhibitory conductances, and stronger inhibitory than excitatory conductances (i.e. approximately balanced synaptic currents). Using these models, we show that balanced synaptic currents evoke fewer spikes per second than excitatory inputs alone or equal excitatory and inhibitory conductances. However, spikes evoked by balanced synaptic inputs are more informative (bits/spike), so that spike trains evoked by all three regimes have similar information rates (bits/s). Consequently, because spikes dominate the energy consumption of our computational models, approximately balanced synaptic currents are also more energy efficient thanmore » other synaptic regimes. Thus, by producing fewer, more informative spikes approximately balanced synaptic currents in cortical neurons can promote both coding efficiency and energy efficiency.« less

Authors:
 [1];  [2];  [3]
  1. Univ. College London, London (United Kingdom). Wellcome Trust Centre for Neuroimaging; Indian Inst. of Science, Bangalore (India). Centre for Neuroscience
  2. Univ. of Cambridge (United Kingdom). Dept. of Zoology
  3. Univ. of Sussex, Falmer (United Kingdom). School of Life Sciences and Centre for Computational Neuroscience and Robotics
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); UT-Battelle LLC/ORNL, Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1565245
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Computational Biology (Online)
Additional Journal Information:
Journal Name: PLoS Computational Biology (Online); Journal Volume: 9; Journal Issue: 10; Journal ID: ISSN 1553-7358
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biochemistry & Molecular Biology; Mathematical & Computational Biology

Citation Formats

Sengupta, Biswa, Laughlin, Simon B., and Niven, Jeremy E. Balanced Excitatory and Inhibitory Synaptic Currents Promote Efficient Coding and Metabolic Efficiency. United States: N. p., 2013. Web. doi:10.1371/journal.pcbi.1003263.
Sengupta, Biswa, Laughlin, Simon B., & Niven, Jeremy E. Balanced Excitatory and Inhibitory Synaptic Currents Promote Efficient Coding and Metabolic Efficiency. United States. doi:10.1371/journal.pcbi.1003263.
Sengupta, Biswa, Laughlin, Simon B., and Niven, Jeremy E. Thu . "Balanced Excitatory and Inhibitory Synaptic Currents Promote Efficient Coding and Metabolic Efficiency". United States. doi:10.1371/journal.pcbi.1003263. https://www.osti.gov/servlets/purl/1565245.
@article{osti_1565245,
title = {Balanced Excitatory and Inhibitory Synaptic Currents Promote Efficient Coding and Metabolic Efficiency},
author = {Sengupta, Biswa and Laughlin, Simon B. and Niven, Jeremy E.},
abstractNote = {A balance between excitatory and inhibitory synaptic currents is thought to be important for several aspects of information processing in cortical neurons in vivo, including gain control, bandwidth and receptive field structure. These factors will affect the firing rate of cortical neurons and their reliability, with consequences for their information coding and energy consumption. Yet how balanced synaptic currents contribute to the coding efficiency and energy efficiency of cortical neurons remains unclear. We used single compartment computational models with stochastic voltage-gated ion channels to determine whether synaptic regimes that produce balanced excitatory and inhibitory currents have specific advantages over other input regimes. Specifically, we compared models with only excitatory synaptic inputs to those with equal excitatory and inhibitory conductances, and stronger inhibitory than excitatory conductances (i.e. approximately balanced synaptic currents). Using these models, we show that balanced synaptic currents evoke fewer spikes per second than excitatory inputs alone or equal excitatory and inhibitory conductances. However, spikes evoked by balanced synaptic inputs are more informative (bits/spike), so that spike trains evoked by all three regimes have similar information rates (bits/s). Consequently, because spikes dominate the energy consumption of our computational models, approximately balanced synaptic currents are also more energy efficient than other synaptic regimes. Thus, by producing fewer, more informative spikes approximately balanced synaptic currents in cortical neurons can promote both coding efficiency and energy efficiency.},
doi = {10.1371/journal.pcbi.1003263},
journal = {PLoS Computational Biology (Online)},
number = 10,
volume = 9,
place = {United States},
year = {2013},
month = {10}
}

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Works referenced in this record:

Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex
journal, November 2003


Updated Energy Budgets for Neural Computation in the Neocortex and Cerebellum
journal, March 2012

  • Howarth, Clare; Gleeson, Padraig; Attwell, David
  • Journal of Cerebral Blood Flow & Metabolism, Vol. 32, Issue 7
  • DOI: 10.1038/jcbfm.2012.35

The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding
journal, May 1998


Noise, neural codes and cortical organization
journal, August 1994


The high-conductance state of neocortical neurons in vivo
journal, September 2003

  • Destexhe, Alain; Rudolph, Michael; Paré, Denis
  • Nature Reviews Neuroscience, Vol. 4, Issue 9
  • DOI: 10.1038/nrn1198

Energy limitation as a selective pressure on the evolution of sensory systems
journal, June 2008

  • Niven, J. E.; Laughlin, S. B.
  • Journal of Experimental Biology, Vol. 211, Issue 11
  • DOI: 10.1242/jeb.017574

Determining the Activation Time Course of Synaptic AMPA Receptors from Openings of Colocalized NMDA Receptors
journal, September 1999


Tonic and Spillover Inhibition of Granule Cells Control Information Flow through Cerebellar Cortex
journal, February 2002


Gating multiple signals through detailed balance of excitation and inhibition in spiking networks
journal, March 2009

  • Vogels, Tim P.; Abbott, L. F.
  • Nature Neuroscience, Vol. 12, Issue 4
  • DOI: 10.1038/nn.2276

Input Summation by Cultured Pyramidal Neurons Is Linear and Position-Independent
journal, January 1998


The metabolic cost of neural information
journal, May 1998

  • Laughlin, Simon B.; de Ruyter van Steveninck, Rob R.; Anderson, John C.
  • Nature Neuroscience, Vol. 1, Issue 1
  • DOI: 10.1038/236

Integration of quanta in cerebellar granule cells during sensory processing
journal, April 2004

  • Chadderton, Paul; Margrie, Troy W.; Häusser, Michael
  • Nature, Vol. 428, Issue 6985
  • DOI: 10.1038/nature02442

Energy as a constraint on the coding and processing of sensory information
journal, August 2001


Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons
journal, November 1995

  • Cobb, S. R.; Buhl, E. H.; Halasy, K.
  • Nature, Vol. 378, Issue 6552
  • DOI: 10.1038/378075a0

Inhibition Determines Membrane Potential Dynamics and Controls Action Potential Generation in Awake and Sleeping Cat Cortex
journal, May 2007


Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors
journal, March 2005

  • Farrant, Mark; Nusser, Zoltan
  • Nature Reviews Neuroscience, Vol. 6, Issue 3
  • DOI: 10.1038/nrn1625

Synaptic Energy Use and Supply
journal, September 2012


Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells: Feed-forward inhibition in the cerebellar cortex
journal, February 2005


Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex
journal, July 2010

  • London, Michael; Roth, Arnd; Beeren, Lisa
  • Nature, Vol. 466, Issue 7302
  • DOI: 10.1038/nature09086

Synaptic background activity influences spatiotemporal integration in single pyramidal cells.
journal, December 1991

  • Bernander, O.; Douglas, R. J.; Martin, K. A.
  • Proceedings of the National Academy of Sciences, Vol. 88, Issue 24
  • DOI: 10.1073/pnas.88.24.11569

Information theory and neural coding
journal, November 1999

  • Borst, Alexander; Theunissen, Frédéric E.
  • Nature Neuroscience, Vol. 2, Issue 11
  • DOI: 10.1038/14731

Neuronal Circuits of the Neocortex
journal, July 2004


Characterizing the sparseness of neural codes
journal, January 2001


The Upward Bias in Measures of Information Derived from Limited Data Samples
journal, March 1995


How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate
journal, June 1999

  • Stemmler, Martin; Koch, Christof
  • Nature Neuroscience, Vol. 2, Issue 6
  • DOI: 10.1038/9173

Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons
journal, November 2001


Gating of Signal Propagation in Spiking Neural Networks by Balanced and Correlated Excitation and Inhibition
journal, November 2010


Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation
journal, May 2003


Recurrent neuronal circuits in the neocortex
journal, July 2007


Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex
journal, September 2005

  • Wilent, W. Bryan; Contreras, Diego
  • Nature Neuroscience, Vol. 8, Issue 10
  • DOI: 10.1038/nn1545

Interneuron Diversity series: Fast in, fast out – temporal and spatial signal processing in hippocampal interneurons
journal, January 2004

  • Jonas, Peter; Bischofberger, Josef; Fricker, Desdemona
  • Trends in Neurosciences, Vol. 27, Issue 1
  • DOI: 10.1016/j.tins.2003.10.010

Dendritic integration of excitatory synaptic input
journal, December 2000

  • Magee, Jeffrey C.
  • Nature Reviews Neuroscience, Vol. 1, Issue 3
  • DOI: 10.1038/35044552

An Energy Budget for Signaling in the Grey Matter of the Brain
journal, October 2001


The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs
journal, December 1992


Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity
journal, April 2004


Reproducibility and Variability in Neural Spike Trains
journal, March 1997


Firing behaviour in a stochastic nerve membrane model based upon the Hodgkin-Huxley equations
journal, December 1979


Information and Efficiency in the Nervous System—A Synthesis
journal, July 2013


Experimental evidence for sparse firing in the neocortex
journal, June 2012


A quantitative description of membrane current and its application to conduction and excitation in nerve
journal, August 1952


The Cost of Cortical Computation
journal, March 2003


Action Potential Energy Efficiency Varies Among Neuron Types in Vertebrates and Invertebrates
journal, July 2010


Impact of Spontaneous Synaptic Activity on the Resting Properties of Cat Neocortical Pyramidal Neurons In Vivo
journal, March 1998


Arithmetic of Subthreshold Synaptic Summation in a Model CA1 Pyramidal Cell
journal, March 2003


Entropy and Information in Neural Spike Trains
journal, January 1998

  • Strong, S. P.; Koberle, Roland; de Ruyter van Steveninck, Rob R.
  • Physical Review Letters, Vol. 80, Issue 1
  • DOI: 10.1103/PhysRevLett.80.197

Comparison of Langevin and Markov channel noise models for neuronal signal generation
journal, January 2010


Synaptic background activity controls spike transfer from thalamus to cortex
journal, October 2005

  • Wolfart, Jakob; Debay, Damien; Le Masson, Gwendal
  • Nature Neuroscience, Vol. 8, Issue 12
  • DOI: 10.1038/nn1591

The influence of some cations on an adenosine triphosphatase from peripheral nerves
journal, January 1957


Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities
journal, March 2008

  • Okun, Michael; Lampl, Ilan
  • Nature Neuroscience, Vol. 11, Issue 5
  • DOI: 10.1038/nn.2105