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Articles, Systems/Circuits

Cytoarchitectonic and Dynamic Origins of Giant Positive Local Field Potentials in the Dentate Gyrus

Antonio Fernández-Ruiz, Sagrario Muñoz, Miguel Sancho, Julia Makarova, Valeri A. Makarov and Oscar Herreras
Journal of Neuroscience 25 September 2013, 33 (39) 15518-15532; DOI: https://doi.org/10.1523/JNEUROSCI.0338-13.2013
Antonio Fernández-Ruiz
1Department of Systems Neuroscience, Cajal Institute, CSIC, Madrid 28002, Spain,
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Sagrario Muñoz
2Department of Applied Physics III, Faculty of Physics, Universidad Complutense de Madrid, Madrid 28040, Spain, and
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Miguel Sancho
2Department of Applied Physics III, Faculty of Physics, Universidad Complutense de Madrid, Madrid 28040, Spain, and
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Julia Makarova
1Department of Systems Neuroscience, Cajal Institute, CSIC, Madrid 28002, Spain,
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Valeri A. Makarov
3Department of Applied Mathematics, Faculty of Mathematics, Universidad Complutense de Madrid, Madrid 28040, Spain
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Oscar Herreras
1Department of Systems Neuroscience, Cajal Institute, CSIC, Madrid 28002, Spain,
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Abstract

To determine why some pathways but not others produce sizable local field potentials (LFPs) and how far from the source can these be recorded, complementary experimental analyses and realistic modeling of specific brain structures are required. In the present study, we combined multiple in vivo linear recordings in rats and a tridimensional finite element model of the dentate gyrus, a curved structure displaying abnormally large positive LFPs. We demonstrate that the polarized dendritic arbour of granule cells (GCs), combined with the curved layered configuration of the population promote the spatial clustering of GC currents in the interposed hilus and project them through the open side at a distance from cell domains. LFPs grow up to 20 times larger than observed in synaptic sites. The dominant positive polarity of hilar LFPs was only produced by the synchronous activation of GCs in both blades by either somatic inhibition or dendritic excitation. Moreover, the corresponding anatomical pathways must project to both blades of the dentate gyrus as even a mild decrease in the spatial synchronization resulted in a dramatic reduction in LFP power in distant sites, yet not in the GC domains. It is concluded that the activation of layered structures may establish sharply delimited spatial domains where synaptic currents from one or another input appear to be segregated according to the topology of afferent pathways and the cytoarchitectonic features of the target population. These also determine preferred directions for volume conduction in the brain, of relevance for interpretation of surface EEG recordings.

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The Journal of Neuroscience: 33 (39)
Journal of Neuroscience
Vol. 33, Issue 39
25 Sep 2013
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Cytoarchitectonic and Dynamic Origins of Giant Positive Local Field Potentials in the Dentate Gyrus
Antonio Fernández-Ruiz, Sagrario Muñoz, Miguel Sancho, Julia Makarova, Valeri A. Makarov, Oscar Herreras
Journal of Neuroscience 25 September 2013, 33 (39) 15518-15532; DOI: 10.1523/JNEUROSCI.0338-13.2013

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Cytoarchitectonic and Dynamic Origins of Giant Positive Local Field Potentials in the Dentate Gyrus
Antonio Fernández-Ruiz, Sagrario Muñoz, Miguel Sancho, Julia Makarova, Valeri A. Makarov, Oscar Herreras
Journal of Neuroscience 25 September 2013, 33 (39) 15518-15532; DOI: 10.1523/JNEUROSCI.0338-13.2013
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