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Parallel Computational Subunits in Dentate Granule Cells Generate Multiple Place Fields

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  • Balázs Ujfalussy
  • Tamás Kiss
  • Péter Érdi

Abstract

A fundamental question in understanding neuronal computations is how dendritic events influence the output of the neuron. Different forms of integration of neighbouring and distributed synaptic inputs, isolated dendritic spikes and local regulation of synaptic efficacy suggest that individual dendritic branches may function as independent computational subunits. In the present paper, we study how these local computations influence the output of the neuron. Using a simple cascade model, we demonstrate that triggering somatic firing by a relatively small dendritic branch requires the amplification of local events by dendritic spiking and synaptic plasticity. The moderately branching dendritic tree of granule cells seems optimal for this computation since larger dendritic trees favor local plasticity by isolating dendritic compartments, while reliable detection of individual dendritic spikes in the soma requires a low branch number. Finally, we demonstrate that these parallel dendritic computations could contribute to the generation of multiple independent place fields of hippocampal granule cells.Author Summary: Neurons were originally divided into three morphologically distinct compartments: the dendrites receive the synaptic input, the soma integrates it and communicates the output of the cell to other neurons via the axon. Although several lines of evidence challenged this oversimplified view, neurons are still considered to be the basic information processing units of the nervous system as their output reflects the computations performed by the entire dendritic tree. In the present study, the authors build a simplified computational model and calculate that, in certain neurons, relatively small dendritic branches are able to independently trigger somatic firing. Therefore, in these cells, an action potential mirrors the activity of a small dendritic subunit rather than the input arriving to the whole dendritic tree. These neurons can be regarded as a network of a few independent integrator units connected to a common output unit. The authors demonstrate that a moderately branched dendritic tree of hippocampal granule cells may be optimized for these parallel computations. Finally the authors show that these parallel dendritic computations could explain some aspects of the location dependent activity of hippocampal granule cells.

Suggested Citation

  • Balázs Ujfalussy & Tamás Kiss & Péter Érdi, 2009. "Parallel Computational Subunits in Dentate Granule Cells Generate Multiple Place Fields," PLOS Computational Biology, Public Library of Science, vol. 5(9), pages 1-16, September.
  • Handle: RePEc:plo:pcbi00:1000500
    DOI: 10.1371/journal.pcbi.1000500
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    References listed on IDEAS

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    1. Christoph Schmidt-Hieber & Peter Jonas & Josef Bischofberger, 2004. "Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus," Nature, Nature, vol. 429(6988), pages 184-187, May.
    2. Jackie Schiller & Guy Major & Helmut J. Koester & Yitzhak Schiller, 2000. "NMDA spikes in basal dendrites of cortical pyramidal neurons," Nature, Nature, vol. 404(6775), pages 285-289, March.
    3. Torkel Hafting & Marianne Fyhn & Sturla Molden & May-Britt Moser & Edvard I. Moser, 2005. "Microstructure of a spatial map in the entorhinal cortex," Nature, Nature, vol. 436(7052), pages 801-806, August.
    4. Nace L. Golding & Nathan P. Staff & Nelson Spruston, 2002. "Dendritic spikes as a mechanism for cooperative long-term potentiation," Nature, Nature, vol. 418(6895), pages 326-331, July.
    5. Attila Losonczy & Judit K. Makara & Jeffrey C. Magee, 2008. "Compartmentalized dendritic plasticity and input feature storage in neurons," Nature, Nature, vol. 452(7186), pages 436-441, March.
    6. Yousheng Shu & Andrea Hasenstaub & David A. McCormick, 2003. "Turning on and off recurrent balanced cortical activity," Nature, Nature, vol. 423(6937), pages 288-293, May.
    7. Christopher D. Harvey & Karel Svoboda, 2007. "Locally dynamic synaptic learning rules in pyramidal neuron dendrites," Nature, Nature, vol. 450(7173), pages 1195-1200, December.
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    Cited by:

    1. Romain Daniel Cazé & Mark Humphries & Boris Gutkin, 2013. "Passive Dendrites Enable Single Neurons to Compute Linearly Non-separable Functions," PLOS Computational Biology, Public Library of Science, vol. 9(2), pages 1-15, February.
    2. Michalis Pagkalos & Spyridon Chavlis & Panayiota Poirazi, 2023. "Introducing the Dendrify framework for incorporating dendrites to spiking neural networks," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Trygve Solstad & Hosam N Yousif & Terrence J Sejnowski, 2014. "Place Cell Rate Remapping by CA3 Recurrent Collaterals," PLOS Computational Biology, Public Library of Science, vol. 10(6), pages 1-10, June.

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