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The link between impact-induced tensile strain and dendritic spine morphology in porcine brain tissue

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  • Brendan Hoffe
  • Gia Kang
  • Hannah Thomson
  • Rohan Banton
  • Thuvan Piehler
  • Oren E Petel
  • Matthew R Holahan

Abstract

Brain tissue as a material presents unique properties with a multitude of cell types and densities, varying degrees of axonal fiber diameters and blood vessels. These neural components are contained within a very viscous environment that upon impact, can result in a variety of tensile, compressive and rotational forces. The depths of the sulcus appear to be particularly vulnerable to biomechanical forces following an impact. The movement and subsequent forces loaded on to the brain have been shown to produce a variety of biomechanical responses that impair neurophysiological functioning at the cellular level. We recently reported a decrease in microtubule associated protein 2 (MAP2) within the depths of the porcine sulcus in an ex vivo model, along with elevated tensile strain in this region within 1 hour after impact. In the current work, using the same impact model, we explored whether changes in spine morphology and density occurred within the same timeframe following impact. The Golgi-Cox method was used to visualize dendritic spine morphology. Cortical pyramidal neurons within the depths and the arms of the sulcus were reconstructed. One hour after impact, there was a change in the distribution of spine type resulting in an increased proportion of mushroom-type spines compared to nonimpacted tissue. The increased proportion of mushroom-type spines was proportional to tensile strain measurements in the apical dendrites. These results demonstrate the sensitivity of dendritic spine morphology to tensile strain within the porcine cortex and suggest a state of hyperexcitability during the hyperacute phase following an impact.

Suggested Citation

  • Brendan Hoffe & Gia Kang & Hannah Thomson & Rohan Banton & Thuvan Piehler & Oren E Petel & Matthew R Holahan, 2025. "The link between impact-induced tensile strain and dendritic spine morphology in porcine brain tissue," PLOS ONE, Public Library of Science, vol. 20(2), pages 1-19, February.
  • Handle: RePEc:plo:pone00:0318932
    DOI: 10.1371/journal.pone.0318932
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