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@INPROCEEDINGS{MoralesGregorio:916175,
      author       = {Morales-Gregorio, Aitor and Kleinjohann, Alexander and Ito,
                      Junji and Albers, Jasper and Fischer, Kirsten and Grün,
                      Sonja and van Albada, Sacha},
      title        = {{O}scillating neural activity saves energy via reduced
                      {N}a+ ion flux},
      reportid     = {FZJ-2022-05995},
      year         = {2022},
      abstract     = {Neural oscillations are ubiquitous in the nervous system
                      and have been shown to enable efficient communi-cation
                      between cortical areas [1]. However, some brain regions tend
                      to show oscillatory activity when theputative amount of
                      information to be transmitted is low, such as the
                      electroencephalography (EEG) of thevisual cortex oscillating
                      at ~10 Hz when the eyes are closed and no visual input is
                      received [2]. To the bestof our knowledge, it is unclear
                      whether there are any practical benefits from such
                      low-frequency oscillationsassociated with reduced
                      information transmission.Here, we hypothesize that
                      synchronous oscillations at low frequencies can reduce the
                      energy consumptionof neurons when compared to asynchronous
                      activity, assuming the same total amount of spikes. We
                      proposethat energy expenditure is decreased through the
                      coordinated flux of ions (especially Na + ) between the
                      intra-and extracellular space, leading to ion concentration
                      gradients that are favorable for reducing the energyconsumed
                      by ion pumps. The saved energy may be considerable because
                      neuronal Na-K pumps consume upto $40\%$ of the total energy
                      in the brain [3, 4].To test our hypothesis, we set up an in
                      silico experiment using a modified Hodgkin-Huxley model
                      whichaccounts for both intra- and extracellular ion
                      concentrations with biologically realistic parameters [5].
                      First,we extended the model to account for a small
                      population of neurons (N=10) with a shared extracellular
                      space.Then, we simulated our model in two different
                      conditions (with approximately the same amount of
                      spikes)using different types of input to the neurons: 1) an
                      inhomogeneous Poisson process with an oscillating
                      rate(oscillatory condition); 2) a Poisson process with a
                      constant rate (non-oscillatory condition). We observed
                      thatthe total Na + flux from the intracellular to the
                      extracellular space was around $20\%$ lower for the
                      oscillatorycondition, i.e. less Na + had to be pumped out of
                      the neurons and thus less energy was needed. We
                      consideredspike waveforms as potential indirect evidence of
                      altered Na + currents between the two conditions. Wemeasured
                      the waveform height and width in silico from our model, and
                      in vivo from extracellular recordingsof macaque visual
                      cortex neurons [6]. However, both the computational model
                      and the in vivo data showeda strong robustness of spike
                      waveforms to the presence of oscillations, despite the large
                      ion flux distortionsrevealed by the model.In conclusion, our
                      computational model suggests that neural oscillations save
                      energy due to favorable Na +gradients, but we could not test
                      this hypothesis using the available in vivo data since the
                      action potentialwaveforms appear unchanged by the altered Na
                      + flux. Future work may consider more direct measurementsof
                      Na + concentrations in vitro or in vivo to test whether the
                      proposed mechanism is at work.References:[1] Sengupta et al.
                      (2013). PLoS Comput. Biol.
                      doi.org/10.1371/journal.pcbi.1003263[2] Lewine and Orrison
                      (1995). doi.org/10.1016/B978-0-8151-6509-5.50012-6[3]
                      Attwell and Laughlin (2001). J. Cereb. Blood Flow Metab.
                      doi.org/10.1097/00004647-200110000-00001[4] Harris et al.
                      (2012). Neuron. doi.org/10.1016/j.neuron.2012.08.019[5]
                      Hübel and Dahlem (2014). PLoS Comput. Biol.
                      doi.org/10.1371/journal.pcbi.1003941[6] Chen et al. (2022).
                      Scientific Data. doi.org/10.1038/s41597-022-01180-1},
      month         = {Oct},
      date          = {2022-10-18},
      organization  = {INM-IBI Retreat, Juelich (Germany), 18
                       Oct 2022 - 19 Oct 2022},
      subtyp        = {After Call},
      cin          = {INM-6 / IAS-6 / INM-10},
      cid          = {I:(DE-Juel1)INM-6-20090406 / I:(DE-Juel1)IAS-6-20130828 /
                      I:(DE-Juel1)INM-10-20170113},
      pnm          = {5231 - Neuroscientific Foundations (POF4-523) / HBP SGA3 -
                      Human Brain Project Specific Grant Agreement 3 (945539)},
      pid          = {G:(DE-HGF)POF4-5231 / G:(EU-Grant)945539},
      typ          = {PUB:(DE-HGF)24},
      url          = {https://juser.fz-juelich.de/record/916175},
}