Susceptibility of primary sensory cortex to spreading depolarizations

Volodymyr B. Bogdanov, Natalie A. Middleton, Jeremy J. Theriot, Patrick D. Parker, Osama M. Abdullah, Y. Sungtaek Ju, Jed A. Hartings, K. C. Brennan

Research output: Contribution to journalArticlepeer-review

Abstract

Spreading depolarizations (SDs) are recognized as actors in neurological disorders as diverse as migraine and traumatic brain injury (TBI). Migraine aura involves sensory percepts, suggesting that sensory cortices might be intrinsically susceptible to SDs. We used optical imaging, MRI, and field potential and potassium electrode recordings in mice and electrocorticographic recordings in humans to determine the susceptibility of different brain regions to SDs. Optical imaging experiments in mice under isoflurane anesthesia showed that both cortical spreading depression and terminal anoxic depolarization arose preferentially in the whisker barrel region of parietal sensory cortex. MRI recordings under isoflurane, ketamine/xylazine, ketamine/isoflurane, and urethane anesthesia demonstrated that the depolarizations did not propagate from a subcortical source. Potassium concentrations showed larger increases in sensory cortex, suggesting a mechanism of susceptibility. Sensory stimulation biased the timing but not the location of depolarization onset. In humans with TBI, there was a trend toward increased incidence of SDs in parietal/temporal sensory cortex compared with other regions. In conclusion, SDs are inducible preferentially in primary sensory cortex in mice and most likely in humans. This tropism can explain the predominant sensory phenomenology of migraine aura. It also demonstrates that sensory cortices are vulnerable in brain injury.

Original languageEnglish (US)
Pages (from-to)4733-4743
Number of pages11
JournalJournal of Neuroscience
Volume36
Issue number17
DOIs
StatePublished - Apr 27 2016

Keywords

  • Anoxic depolarization
  • Cortical spreading depression
  • Migraine
  • Sensory cortex
  • Traumatic brain injury

ASJC Scopus subject areas

  • Neuroscience(all)

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