Hypoxia-ischemia (HI) injury in neonatal animals leads to selective regional loss of neurons including CA1 and CA3 pyramidal neurons of the hippocampus as well as nonlethal pathologies. Glutamate-receptor over-activation and Ca2+ influx are involved in these neonatal changes. We examined glutamate-evoked Ca2+ responses in neonatal (PN 7-13) and young adult (PN 21-27) CA1 pyramidal neurons in acute slices from rats. In neonates, transient exposure to glutamate produced large Ca2+ increases throughout neurons, including distal dendrites (primary Ca2+ responses). Repeated exposures resulted in sustained Ca2+ increases in apical dendrites (secondary Ca2+ responses) that were independent of continued glutamate exposure. These responses propagated and invaded the soma, resulting in irrecoverably high Ca2+ elevations. In neurons from adults, identical glutamate exposure evoked primary Ca2+ responses only in somata and proximal apical dendrites. Repeated glutamate exposures in the adult neurons also led to secondary Ca2+ responses, but they arose in the peri-somatic region and then spread outward to distal apical dendrites, again without recovery. More stimuli were required to initiate secondary responses in neurons from adult versus neonates. Block of GABAA receptors in adults caused the primary and secondary responses to revert to the spatial pattern seen in the neonates and greatly increased their vulnerability to glutamate. These findings suggest that neurodegenerative secondary Ca2+ events may be important determinants of susceptibility to HI injury in the developing CNS and that immature CA1 neurons may be more susceptible to excitotoxic injury due at least in part to insufficient development of GABAergic inputs to their dendrites.

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