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The Journal of Neuroscience, September 29, 2004, 24(39):8470-8479; doi:10.1523/JNEUROSCI.1413-04.2004

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Behavioral/Systems/Cognitive
Phase Segregation of Medial Septal GABAergic Neurons during Hippocampal Theta Activity

Zsolt Borhegyi,^1 * Viktor Varga,^1 * Nóra Szilágyi,² Dániel Fabo,¹ and Tamás F. Freund¹

¹Department of Cellular and Network Neurobiology, Institute of Experimental Medicine of the Hungarian Academy of Science, Budapest 1083, Hungary, and ²Department of Physiology and Neurobiology, Eötvös Loránd University of Sciences, Budapest 1117, Hungary

Septo-hippocampal GABAergic neurons immunoreactive for parvalbumin are thought to play a crucial role in the generation of hippocampal theta oscillations associated with a specific stage of memory formation. Here we use in vivo juxtacellular recording and filling in the medial septum followed by immunocytochemical identification of the recorded cells containing parvalbumin to determine their firing pattern, phase relationship with hippocampal theta, morphology, and to thereby reveal their involvement in the generation of hippocampal theta activity. We have demonstrated that GABAergic medial septal neurons form two distinct populations exhibiting highly regular bursting activity that is tightly coupled to either the trough (178°) or the peak (330°) of hippocampal theta waves. Additionally, different types of bursting as well as nonbursting activity patterns were also observed. The morphological reconstruction of theta-bursting neurons revealed extensive axon arbors of these cells with numerous local collaterals establishing symmetrical synapses; thus, synchrony among the septal pacemaker units may be brought about by their recurrent collateral interactions. Long projecting axons could also be found running dorsally toward the hippocampus and ventrally in the direction of basal forebrain regions. We conclude that GABAergic neurons in the medial septum, which are known to selectively innervate hippocampal interneurons, are in a position to induce rhythmic disinhibition in the hippocampus and other theta-related subcortical areas at two different phases of hippocampal theta.

Key words: EEG; juxtacellular; wavelet; parvalbumin; burst; immunocytochemistry

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Received April 15, 2004; revised July 8, 2004; accepted July 28, 2004.

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