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Three-dimensional spatial modeling of spines along dendritic networks in human cortical pyramidal neurons

Author

Listed:
  • Laura Anton-Sanchez
  • Pedro Larrañaga
  • Ruth Benavides-Piccione
  • Isabel Fernaud-Espinosa
  • Javier DeFelipe
  • Concha Bielza

Abstract

We modeled spine distribution along the dendritic networks of pyramidal neurons in both basal and apical dendrites. To do this, we applied network spatial analysis because spines can only lie on the dendritic shaft. We expanded the existing 2D computational techniques for spatial analysis along networks to perform a 3D network spatial analysis. We analyzed five detailed reconstructions of adult human pyramidal neurons of the temporal cortex with a total of more than 32,000 spines. We confirmed that there is a spatial variation in spine density that is dependent on the distance to the cell body in all dendrites. Considering the dendritic arborizations of each pyramidal cell as a group of instances of the same observation (the neuron), we used replicated point patterns together with network spatial analysis for the first time to search for significant differences in the spine distribution of basal dendrites between different cells and between all the basal and apical dendrites. To do this, we used a recent variant of Ripley’s K function defined to work along networks. The results showed that there were no significant differences in spine distribution along basal arbors of the same neuron and along basal arbors of different pyramidal neurons. This suggests that dendritic spine distribution in basal dendritic arbors adheres to common rules. However, we did find significant differences in spine distribution along basal versus apical networks. Therefore, not only do apical and basal dendritic arborizations have distinct morphologies but they also obey different rules of spine distribution. Specifically, the results suggested that spines are more clustered along apical than in basal dendrites. Collectively, the results further highlighted that synaptic input information processing is different between these two dendritic domains.

Suggested Citation

  • Laura Anton-Sanchez & Pedro Larrañaga & Ruth Benavides-Piccione & Isabel Fernaud-Espinosa & Javier DeFelipe & Concha Bielza, 2017. "Three-dimensional spatial modeling of spines along dendritic networks in human cortical pyramidal neurons," PLOS ONE, Public Library of Science, vol. 12(6), pages 1-14, June.
  • Handle: RePEc:plo:pone00:0180400
    DOI: 10.1371/journal.pone.0180400
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    References listed on IDEAS

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    1. Adrian Baddeley & Aruna Jammalamadaka & Gopalan Nair, 2014. "Multitype point process analysis of spines on the dendrite network of a neuron," Journal of the Royal Statistical Society Series C, Royal Statistical Society, vol. 63(5), pages 673-694, November.
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    4. Ute Hahn, 2012. "A Studentized Permutation Test for the Comparison of Spatial Point Patterns," Journal of the American Statistical Association, Taylor & Francis Journals, vol. 107(498), pages 754-764, June.
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    6. Baddeley, Adrian & Turner, Rolf, 2005. "spatstat: An R Package for Analyzing Spatial Point Patterns," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 12(i06).
    7. Qi Wei Ang & Adrian Baddeley & Gopalan Nair, 2012. "Geometrically Corrected Second Order Analysis of Events on a Linear Network, with Applications to Ecology and Criminology," Scandinavian Journal of Statistics, Danish Society for Theoretical Statistics;Finnish Statistical Society;Norwegian Statistical Association;Swedish Statistical Association, vol. 39(4), pages 591-617, December.
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