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Brain Research Institute, University of Zurich, CH-8057 Zurich, Switzerland
Oscillatory activity characterizes the activity of the hippocampus in vivo; however, the underlying mechanism remains unknown. It is also known that during oscillations the number of action potentials provided by the principal cells is surprisingly low, and it is still an open question how oscillations can emerge under such constraints. One suggestion is that the discharge activity of inhibitory cells takes this function; however, this has been found, in my previous studies, not to be the case for cholinergically mediated and intrinsically generated hippocampal oscillations. This study identifies the hippocampal intrinsic network oscillator and the interactions which underlie the concurrent expression of cholinergically mediated theta (4–15 Hz) and gamma (20–80 Hz) oscillations. A particular axonal network that involves the hippocampal associative pathway, shown to consist of axonal collaterals of CA2 and some CA3 pyramidal cells, forms the oscillator core element. It is functionally activated via two cholinergically mediated reactions. First, direct activation of CA2 and CA3 pyramidal cells to discharge. Second, enhancement of gap junction-mediated axo-axonic interactions among axons of the core element and associated axons of interneurones, which together form the full oscillator. With these two reactions it is possible to explain the rhythmicities and patterns of activity, under the condition of a low number of action potentials. The discharge of CA3 pyramidals serves mainly as a trigger, while firing by CA2 pyramidals, and to a lesser degree by CA3 pyramidals, maintains the oscillatory activity. The cholinergically mediated 2-fold increase in axonal gap junction communication between cells serves two functions: (a) creation of specific activation pathways to produce the rhythmicities and patterns, and (b) formation of a reverberatory system that extends the time during which the sparsely generated action potentials can interact in the network, thereby providing a new source of action potentials, critical for the expression of oscillatory activity.
(Received 22 September 2003;
accepted after revision 22 October 2003;
first published online 31 October 2003)
Corresponding author Y. Fischer: Brain Research Institute, University of Zurich, CH-8057 Zurich, Switzerland. Email: kfischer{at}hifo.unizh.ch
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