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Research ArticleTheory, Sensory and Motor Systems

Up-Down-Like Background Spiking Can Enhance Neural Information Transmission

Felix Droste and Benjamin Lindner
eNeuro 27 December 2017, 4 (6) ENEURO.0282-17.2017; https://doi.org/10.1523/ENEURO.0282-17.2017
Felix Droste
1 Bernstein Center for Computational Neuroscience, Berlin 10115, Germany
2Department of Physics, Humboldt Universität zu Berlin, Berlin 12489, Germany
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Benjamin Lindner
1 Bernstein Center for Computational Neuroscience, Berlin 10115, Germany
2Department of Physics, Humboldt Universität zu Berlin, Berlin 12489, Germany
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  • Figure 1.
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    Figure 1.

    How do the transmission properties of the readout population depend on the activity of the background population? 1000 uncoupled neurons receive a common signal. We ask how the information transmission between the signal and the activity of this readout population is influenced by the dynamic regime of the background population. In particular, we compare a regime where background spikes occur uniformly in time to one where they have been redistributed into up states.

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    Figure 2.

    More information about the signal can be transmitted by the readout population activity a(t) if background activity undergoes transitions between up and down states. A, B, Firing rate of the background population and raster-plot of the spikes received by an arbitrary readout neuron. C, D, Signal realization (frozen noise). E, F, Normalized population activity Embedded Image and spike raster of the readout population. For the population activity, two trials with the same signal (C, D) and, in the UD case, two-state process (B) are shown. G, Coherence between signal and activity of the readout population. H, Lower bound to the mutual information rate and Embedded Image, the mean firing rate of the readout population, as a function of the mean background rate Embedded Image . The dashed line marks the Embedded Image value used in A–G. Parameters, if not indicated otherwise: Embedded Image Hz, Embedded Image ms, Embedded Image ms.

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    Figure 3.

    Effects of up/down duration and temporal structure of the signal. A, Coherence for AI background (blue) and UD background at three different values for the mean duration Embedded Image. Here, Embedded Image Hz. B, Mutual information rates as a function of the background rate for the cases shown in A. The inset shows the theoretical curves over a wider range; the gray line marks what could optimally be reached by infinitely slow switching. C, D, Signal power spectra and coherence for a lower cutoff f0 of 0 Hz and 25 Hz, respectively. E, Mutual information rates as a function of f0. The dashed line marks cutoff frequency used in A–C. In A–E, Embedded Image ms, Embedded Image ms, Embedded Image Hz.

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    Figure 4.

    The beneficial effect of a UD background persists in a more realistic setup. A, Sketch of the modified setup. B, Mutual information rate for different mean background rates Embedded Image. The dashed line marks the value used in C–F. C, Sample traces of the readout population activity for irregular (gray, Embedded Image) and rather regular (red, Embedded Image) UD switching. D, Histogram for the duration of up states in the readout population. To obtain this, population activity is binned (width ΔT = 10 ms); n consecutive bins in each of which at least one readout neuron spikes then define a readout up state of length TU = nΔT. E, Effect of changing the regularity of UD switching on the mutual information rate. F, Effect of changing the recurrent synaptic weights. The dotted line marks the value used in B–E. In all panels, Embedded Image ms.

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    Figure 5.

    A simple model for the effect of the signal on the UD switching We assume that the transition rates between UD states in the background are modulated by the signal. Shown is a realization of the signal and the corresponding background rate for three values of the modulation strength Embedded Image, as well as the mutual information rate over the mean background rate (obtained in simulations) for these Embedded Image. A, Parameters as in Figure 2. B, A much slower signal with fC = 1 Hz. Note the different y-axis scaling in the mutual information plots.

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    Figure 6.

    Traveling up states allow continuous signal transmission A, Sketch of the setup. B, Activity and spike raster of the readout population (neurons ordered by the position of their background population). C, Mutual information rates for different background rates. Red solid and dashed lines correspond to the theoretical limits Embedded Image and Embedded Image , respectively; blue line is theory for AI background. The black dashed line marks the background rate used in the other panels. D, Mutual information rates for varying wave speed c. The dotted line marks the wave speed used in B, C. E, Silence density, i.e., fraction of time bins (length ΔT = 4 ms) in which the population activity is zero. Where nothing else is indicated, the wave speed is c = 10 mm/s and the mean background rate is Embedded Image Hz. In C–E, symbols represent simulation results, while lines are theory.

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    Figure 7.

    What do our results say about the comparison of different brain states? A, We consider a switch from an attentive state (1) to an inattentive state at a lower mean background firing rate Embedded Image. The background rate can either be lowered by introducing pauses (going to the UD regime (2)) or in a uniform manner (going to the AI regime (3)). B, Switching from (1) to (2) maintains higher information rates than switching to (3); we propose that this is why (2), not (3), is observed. In both cases, the overall information transmission is reduced. C, This goes along with an increase in noise correlations (correlations among neurons within one trial; shown is the mean Pearson correlation coefficient of spike counts in 100-ms time bins; see Materials and Methods) and (D) a decrease in signal correlations (correlations in the binned population activity across trials; see Materials and Methods). All parameters are chosen like in Figure 6; in B–D, symbols represent simulation results.

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    Table 1.

    Parameters used if not indicated otherwise

    Uncoupled population
    N1000Size of readout population
    τ20 msMembrane time constant
    V 015 mVResting potential
    Embedded Image 1 msRefractory period
    Jext0.1 mVMean weight of background spikes
    Embedded Image 20 mVThreshold voltage
    Embedded Image 10 mVReset voltage
    NB1000Number of background neurons
    Embedded Image 1.35 HzMean background rate
    Embedded Image 333 msMean up state duration
    Embedded Image 200 msMean down state duration
    Embedded Image 1γ Distribution scale parameter
    Embedded Image 0.3 mVSignal standard deviation
    f00 HzLower signal cutoff frequency
    fC75 HzUpper signal cutoff frequency
    Embedded Image 0.1 msSimulation time step
    T4000 msSimulation time for one trial
    Recurrent network (where different from above)
    NS1000Size of signal population
    rS1 HzBaseline rate of signal population
    Embedded Image 0.15Relative rate modulation
    Embedded Image 1.9 HzMean background rate
    Embedded Image 200 msMean up state duration
    Embedded Image 50γ Distribution scale parameter
    NE10,000Size of excitatory population
    NI2500Size of inhibitory population
    J0.1 mVWeight of recurrent connections
    CE1000Number excitatory connections
    CI250Number inhibitory connections
    V011 mVResting potential
    g4.5Relative strength of inhibition
    D1.5 msDelay
    Traveling UD
    l4 mmExtent of background population
    c10 mm/sPropagation speed
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November/December 2017
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Up-Down-Like Background Spiking Can Enhance Neural Information Transmission
Felix Droste, Benjamin Lindner
eNeuro 27 December 2017, 4 (6) ENEURO.0282-17.2017; DOI: 10.1523/ENEURO.0282-17.2017

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Up-Down-Like Background Spiking Can Enhance Neural Information Transmission
Felix Droste, Benjamin Lindner
eNeuro 27 December 2017, 4 (6) ENEURO.0282-17.2017; DOI: 10.1523/ENEURO.0282-17.2017
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Keywords

  • Information Transmission
  • modelling
  • network
  • spontaneous activity
  • up-down States

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