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The Journal of Neuroscience, June 1, 2005, 25(22):5280-5289; doi:10.1523/JNEUROSCI.0378-05.2005
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Development/Plasticity/Repair
Depolarizing GABA Acts on Intrinsically Bursting Pyramidal Neurons to Drive Giant Depolarizing Potentials in the Immature Hippocampus
Sampsa T. Sipilä,1 Kristiina Huttu,1 Ivan Soltesz,3 Juha Voipio,1 andKai Kaila1,2 1Department of Biological and Environmental Sciences and 2Neuroscience Center, University of Helsinki, FIN-00014 Helsinki, Finland, and 3Department of Anatomy and Neurobiology, University of California, Irvine, California 92697-1280
Spontaneous periodic network events are a characteristic feature of developing neuronal networks, and they are thought to play a crucial role in the maturation of neuronal circuits. In the immature hippocampus, these types of events are seen in intracellular recordings as giant depolarizing potentials (GDPs) during the stage of neuronal development when GABAA-mediated transmission is depolarizing. However, the precise mechanism how GABAergic transmission promotes GDP occurrence is not known. Using whole-cell, cell-attached, perforated-patch, and field-potential recordings in hippocampal slices, we demonstrate here that CA3 pyramidal neurons in the newborn rat generate intrinsic bursts when depolarized. Furthermore, the characteristic rhythmicity of GDP generation is not based on a temporally patterned output of the GABAergic interneuronal network. However, GABAergic depolarization plays a key role in promoting voltage-dependent, intrinsic pyramidal bursting activity. The present data indicate that glutamatergic CA3 neurons have an instructive, pacemaker role in the generation of GDPs, whereas both synaptic and tonic depolarizing GABAergic mechanisms exert a temporally nonpatterned, facilitatory action in the generation of these network events.
Key words: GABAergic; network; hippocampus; development; pacemaker; glutamatergic neurons; activity
Received Jan 27, 2005; revised March 24, 2005; accepted April 16, 2005.
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