Energy deprivation transiently enhances rhythmic inhibitory events in the CA3 hippocampal network in vitro

TY - JOUR

T1 - Energy deprivation transiently enhances rhythmic inhibitory events in the CA3 hippocampal network in vitro

AU - Gee, C E

AU - Benquet, P

AU - Demont-Guignard, S

AU - Wendling, F

AU - Gerber, U

N1 - Copyright 2010 IBRO. Published by Elsevier Ltd. All rights reserved.

PY - 2010/7/14

Y1 - 2010/7/14

N2 - Oxygen glucose deprivation (OGD) leads to rapid suppression of synaptic transmission. Here we describe an emergence of rhythmic activity at 8 to 20 Hz in the CA3 subfield of hippocampal slice cultures occurring for a few minutes prior to the OGD-induced cessation of evoked responses. These oscillations, dominated by inhibitory events, represent network activity, as they were abolished by tetrodotoxin. They were also completely blocked by the GABAergic antagonist picrotoxin, and strongly reduced by the glutamatergic antagonist NBQX. Applying CPP to block NMDA receptors had no effect and neither did UBP302, an antagonist of GluK1-containing kainate receptors. The gap junction blocker mefloquine disrupted rhythmicity. Simultaneous whole-cell voltage-clamp recordings from neighboring or distant CA3 pyramidal cells revealed strong cross-correlation of the incoming rhythmic activity. Interneurons in the CA3 area received similar correlated activity. Interestingly, oscillations were much less frequently observed in the CA1 area. These data, together with the observation that the recorded activity consists primarily of inhibitory events, suggest that CA3 interneurons are important for generating these oscillations. This transient increase in inhibitory network activity during OGD may represent a mechanism contributing to the lower vulnerability to ischemic insults of the CA3 area as compared to the CA1 area.

AB - Oxygen glucose deprivation (OGD) leads to rapid suppression of synaptic transmission. Here we describe an emergence of rhythmic activity at 8 to 20 Hz in the CA3 subfield of hippocampal slice cultures occurring for a few minutes prior to the OGD-induced cessation of evoked responses. These oscillations, dominated by inhibitory events, represent network activity, as they were abolished by tetrodotoxin. They were also completely blocked by the GABAergic antagonist picrotoxin, and strongly reduced by the glutamatergic antagonist NBQX. Applying CPP to block NMDA receptors had no effect and neither did UBP302, an antagonist of GluK1-containing kainate receptors. The gap junction blocker mefloquine disrupted rhythmicity. Simultaneous whole-cell voltage-clamp recordings from neighboring or distant CA3 pyramidal cells revealed strong cross-correlation of the incoming rhythmic activity. Interneurons in the CA3 area received similar correlated activity. Interestingly, oscillations were much less frequently observed in the CA1 area. These data, together with the observation that the recorded activity consists primarily of inhibitory events, suggest that CA3 interneurons are important for generating these oscillations. This transient increase in inhibitory network activity during OGD may represent a mechanism contributing to the lower vulnerability to ischemic insults of the CA3 area as compared to the CA1 area.

KW - Animals

KW - CA3 Region, Hippocampal

KW - Gap Junctions

KW - Glucose

KW - In Vitro Techniques

KW - Interneurons

KW - Oxygen

KW - Patch-Clamp Techniques

KW - Periodicity

KW - Pyramidal Cells

KW - Rats

KW - Rats, Wistar

U2 - 10.1016/j.neuroscience.2010.04.021

DO - 10.1016/j.neuroscience.2010.04.021

M3 - SCORING: Journal article

C2 - 20403414

VL - 168

SP - 605

EP - 612

JO - NEUROSCIENCE

JF - NEUROSCIENCE

SN - 0306-4522

IS - 3

ER -