A distinct boundary between the higher brain's susceptibility to ischemia and the lower brain's resistance

PLoS One. 2013 Nov 6;8(11):e79589. doi: 10.1371/journal.pone.0079589. eCollection 2013.

Abstract

Higher brain regions are more susceptible to global ischemia than the brainstem, but is there a gradual increase in vulnerability in the caudal-rostral direction or is there a discrete boundary? We examined the interface between `higher` thalamus and the hypothalamus the using live brain slices where variation in blood flow is not a factor. Whole-cell current clamp recording of 18 thalamic neurons in response to 10 min O2/glucose deprivation (OGD) revealed a rapid anoxic depolarization (AD) from which thalamic neurons do not recover. Newly acquired neurons could not be patched following AD, confirming significant regional thalamic injury. Coinciding with AD, light transmittance (LT) imaging during whole-cell recording showed an elevated LT front that initiated in midline thalamus and that propagated into adjacent hypothalamus. However, hypothalamic neurons patched in paraventricular nucleus (PVN, n= 8 magnocellular and 12 parvocellular neurons) and suprachiasmatic nucleus (SCN, n= 18) only slowly depolarized as AD passed through these regions. And with return to control aCSF, hypothalamic neurons repolarized and recovered their input resistance and action potential amplitude. Moreover, newly acquired hypothalamic neurons could be readily patched following exposure to OGD, with resting parameters similar to neurons not previously exposed to OGD. Thalamic susceptibility and hypothalamic resilience were also observed following ouabain exposure which blocks the Na(+)/K(+) pump, evoking depolarization similar to OGD in all neuronal types tested. Finally, brief exposure to elevated [K(+)]o caused spreading depression (SD, a milder, AD-like event) only in thalamic neurons so SD generation is regionally correlated with strong AD. Therefore the thalamus-hypothalamus interface represents a discrete boundary where neuronal vulnerability to ischemia is high in thalamus (like more rostral neocortex, striatum, hippocampus). In contrast hypothalamic neurons are comparatively resistant, generating weaker and recoverable anoxic depolarization similar to brainstem neurons, possibly the result of a Na/K pump that better functions during ischemia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / pathology
  • Disease Susceptibility
  • Glucose / metabolism
  • Hypothalamus / metabolism
  • Hypothalamus / pathology*
  • Hypothalamus / physiopathology*
  • Ischemia / metabolism
  • Ischemia / pathology*
  • Male
  • Neurons / pathology
  • Oxygen / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Thalamus / metabolism
  • Thalamus / pathology*
  • Thalamus / physiopathology*

Substances

  • Glucose
  • Oxygen

Grants and funding

This work was supported by the Heart and Stroke Foundation of Ontario (grant T- 4478) and the Faculty of Health Sciences, Queen's University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.