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The Journal of Neuroscience, April 9, 2008, 28(15):4096-4107; doi:10.1523/JNEUROSCI.0247-08.2008

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Cellular/Molecular
The Hippocamposeptal Pathway Generates Rhythmic Firing of GABAergic Neurons in the Medial Septum and Diagonal Bands: An Investigation Using a Complete Septohippocampal Preparation In Vitro

Frédéric Manseau, Romain Goutagny, Marc Danik, and Sylvain Williams

Douglas Hospital Research Center, Department of Psychiatry, McGill University, Montreal, Quebec, Canada H4H 1R3

Correspondence should be addressed to Dr. Frederic Manseau, European Brain Research Institute, "Rita Levi-Montalcini" Foundation, Via del Fosso di Fiorano, 64/65, 00143 Rome, Italy. Email: f.manseau{at}ebri.it

The medial septum diagonal band area (MS/DB) projects to the hippocampus through the fornix/fimbria pathway and is implicated in generating hippocampal theta oscillations. The hippocampus also projects back to the MS/DB, but very little is known functionally about this input. Here, we investigated the physiological role of hippocamposeptal feedback to the MS/DB in a complete in vitro septohippocampal preparation containing the intact interconnecting fornix/fimbria pathway. We demonstrated that carbachol-induced rhythmic theta-like hippocampal oscillations recorded extracellularly were synchronized with powerful rhythmic IPSPs in whole-cell recorded MS/DB neurons. Interestingly, we found that these IPSPs evoked rebound spiking in GABAergic MS/DB neurons. In contrast, putative cholinergic and glutamatergic MS/DB neurons responded only weakly with rebound spiking and, as a result, were mostly silent during theta-like oscillations. We next determined the mechanism underlying the rebound spiking that followed the IPSPs in MS/DB GABAergic neurons using phasic electrical stimulation of the fornix/fimbria pathway. We demonstrate that the increased rebound spiking was attributable to the activation of I_h current, because it was significantly reduced by low concentrations of the I_h antagonist ZD7288 [4-(N-ethyl-N-phenylamino)-1,2-dimethyl-6-(methylamino) pyridinium chloride]. Together, these results suggest that rhythmical activity in hippocampus is transferred to the MS/DB and can preferentially phase the spiking of GABAergic MS/DB neurons because of their significant expression of I_h currents. Our data demonstrate that hippocamposeptal inhibition facilitates theta rhythmic discharges in MS/DB GABAergic neurons while favoring the inhibition of most ACh and glutamate neurons.

Key words: medial septum; hippocamposeptal feedback; GABAergic neurons; carbachol; rhythmic inhibition; I_h current; theta oscillation

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Received Sept. 28, 2007; revised March 12, 2008; accepted March 12, 2008.

Correspondence should be addressed to Dr. Frederic Manseau, European Brain Research Institute, "Rita Levi-Montalcini" Foundation, Via del Fosso di Fiorano, 64/65, 00143 Rome, Italy. Email: f.manseau{at}ebri.it

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