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The effect of inhibition on rate code efficiency indicators

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  • Tomas Barta
  • Lubomir Kostal

Abstract

In this paper we investigate the rate coding capabilities of neurons whose input signal are alterations of the base state of balanced inhibitory and excitatory synaptic currents. We consider different regimes of excitation-inhibition relationship and an established conductance-based leaky integrator model with adaptive threshold and parameter sets recreating biologically relevant spiking regimes. We find that given mean post-synaptic firing rate, counter-intuitively, increased ratio of inhibition to excitation generally leads to higher signal to noise ratio (SNR). On the other hand, the inhibitory input significantly reduces the dynamic coding range of the neuron. We quantify the joint effect of SNR and dynamic coding range by computing the metabolic efficiency—the maximal amount of information per one ATP molecule expended (in bits/ATP). Moreover, by calculating the metabolic efficiency we are able to predict the shapes of the post-synaptic firing rate histograms that may be tested on experimental data. Likewise, optimal stimulus input distributions are predicted, however, we show that the optimum can essentially be reached with a broad range of input distributions. Finally, we examine which parameters of the used neuronal model are the most important for the metabolically efficient information transfer.Author summary: Neurons communicate by firing action potentials, which can be considered as all-or-none events. The classical rate coding hypothesis states that neurons communicate the information about stimulus intensity by altering their firing frequency. Cortical neurons typically receive a signal from many different neurons, which, depending on the synapse type, either depolarize (excitatory input) or hyperpolarize (inhibitory input) the neural membrane. We use a neural model with excitatory and inhibitory synaptic conductances to reproduce in-vivo like activity and investigate how the intensity of presynaptic inhibitory activity affects the neuron’s ability to transmit information through rate code. We reach a counter-intuitive result that increase in inhibition improves the signal-to-noise ratio of the neural response, despite introducing additional noise to the input signal. On the other hand, inhibition also limits the neuronal output range. However, in the end, the actual amount of information transmitted (in bits per energy expended) is remarkably robust to the inhibition level present in the system. Our approach also yields predictions in the form of post-synaptic firing rate histograms, which can be compared with in-vivo recordings.

Suggested Citation

  • Tomas Barta & Lubomir Kostal, 2019. "The effect of inhibition on rate code efficiency indicators," PLOS Computational Biology, Public Library of Science, vol. 15(12), pages 1-21, December.
  • Handle: RePEc:plo:pcbi00:1007545
    DOI: 10.1371/journal.pcbi.1007545
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    References listed on IDEAS

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    1. Marie Levakova & Lubomir Kostal & Christelle Monsempès & Vincent Jacob & Philippe Lucas, 2018. "Moth olfactory receptor neurons adjust their encoding efficiency to temporal statistics of pheromone fluctuations," PLOS Computational Biology, Public Library of Science, vol. 14(11), pages 1-17, November.
    2. Evan C. Smith & Michael S. Lewicki, 2006. "Efficient auditory coding," Nature, Nature, vol. 439(7079), pages 978-982, February.
    3. Yasuhiro Tsubo & Yoshikazu Isomura & Tomoki Fukai, 2012. "Power-Law Inter-Spike Interval Distributions Infer a Conditional Maximization of Entropy in Cortical Neurons," PLOS Computational Biology, Public Library of Science, vol. 8(4), pages 1-11, April.
    4. Ryota Kobayashi & Shuhei Kurita & Anno Kurth & Katsunori Kitano & Kenji Mizuseki & Markus Diesmann & Barry J. Richmond & Shigeru Shinomoto, 2019. "Reconstructing neuronal circuitry from parallel spike trains," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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