Enduring effects of early life stress on firing patterns of hippocampal and thalamocortical neurons in rats : implications for limbic epilepsy

Ali, Idrish; O'Brien, Patrick; Kumar, Gaurav; Zheng, Thomas; Jones, Nigel C.; Pinault, Didier; French, Chris; Morris, Margaret J.; Salzberg, Michael R.; O'Brien, Terence J.

doi:10.1371/JOURNAL.PONE.0066962

Title

Enduring effects of early life stress on firing patterns of hippocampal and thalamocortical neurons in rats : implications for limbic epilepsy

Author

Ali, Idrish

O'Brien, Patrick

Kumar, Gaurav

Zheng, Thomas

Jones, Nigel C.

Pinault, Didier

French, Chris

Morris, Margaret J.

Salzberg, Michael R.

O'Brien, Terence J.

Abstract

Early life stress results in an enduring vulnerability to kindling-induced epileptogenesis in rats, but the underlying mechanisms are not well understood. Recent studies indicate the involvement of thalamocortical neuronal circuits in the progression of kindling epileptogenesis. Therefore, we sought to determine in vivo the effects of early life stress and amygdala kindling on the firing pattern of hippocampus as well as thalamic and cortical neurons. Eight week old male Wistar rats, previously exposed to maternal separation (MS) early life stress or early handling (EH), underwent amygdala kindling (or sham kindling). Once fully kindled, in vivo juxtacellular recordings in hippocampal, thalamic and cortical regions were performed under neuroleptic analgesia. In the thalamic reticular nucleus cells both kindling and MS independently lowered firing frequency and enhanced burst firing. Further, burst firing in the thalamic reticular nucleus was significantly increased in kindled MS rats compared to kindled EH rats (p<0.05). In addition, MS enhanced burst firing of hippocampal pyramidal neurons. Following a stimulation-induced seizure, somatosensory cortical neurons exhibited a more pronounced increase in burst firing in MS rats than in EH rats. These data demonstrate changes in firing patterns in thalamocortical and hippocampal regions resulting from both MS and amygdala kindling, which may reflect cellular changes underlying the enhanced vulnerability to kindling in rats that have been exposed to early life stress.

Language

English

Source (journal)

PLoS ONE

Publication

2013

ISSN

1932-6203

DOI

10.1371/JOURNAL.PONE.0066962

Volume/pages

8 :6 (2013) , p. 1-12