Abstract
The neurophysiological processes that can cause theta-to-gamma frequency range (4–80 Hz) network oscillations in the rhinal cortical-hippocampal system and the potential connectivity-based interactions of such forebrain rhythms are a topic of intensive investigation. Here, using selective Channelrhodopsin-2 (ChR2) expression in mouse forebrain glutamatergic cells, we were able to locally, temporally precisely, and reliably induce fast (20–40 Hz) field potential oscillations in hippocampal area CA1 in vitro (at 25°C) and in vivo (i.e., slightly anesthetized NEX-Cre-ChR2 mice). As revealed by pharmacological analyses and patch-clamp recordings from pyramidal cells and GABAergic interneurons in vitro, these light-triggered oscillations can exclusively arise from sustained suprathreshold depolarization (~200 ms or longer) and feedback inhibition of CA1 pyramidal neurons, as being mandatory for prototypic pyramidal-interneuron network (P-I) oscillations. Consistently, the oscillations comprised rhythmically occurring population spikes (generated by pyramidal cells) and their frequency increased with increasing spectral power. We further demonstrate that the optogenetically driven CA1 oscillations, which remain stable over repeated evocations, are impaired by the stress hormone corticotropin-releasing factor (CRF, 125 nM) in vitro and, even more remarkably, found that they are accompanied by concurrent states of enforced theta activity in the memory-associated perirhinal cortex (PrC) in vivo. The latter phenomenon most likely derives from neurotransmission via a known, but poorly studied excitatory CA1→PrC pathway. Collectively, our data provide evidence for the existence of a prototypic (CRF-sensitive) P-I gamma rhythm generator in area CA1 and suggest that CA1 P-I oscillations can rapidly up-regulate theta activity strength in hippocampus-innervated rhinal networks, at least in the PrC.
Highlights
There is overwhelming evidence that several cognitive functions in mammals require theta (4–12 Hz) and/or gamma (30–80 Hz) network oscillations in the hippocampus and associated rhinal cortices, including the perirhinal cortex (PrC; Zola-Morgan et al, 1993; Bilkey and Heinemann, 1999; Fell et al, 2001; Colgin and Moser, 2010; Buzsáki and Wang, 2012)
Two experimentally induced types of this self-produced rhythmicity involve feedback inhibition of pyramidal neurons (Whittington et al, 1997; Buzsáki and Wang, 2012; Pietersen et al, 2014), but it remains unclear whether area CA1 harbors the circuitry for a generation of prototypic pyramidal-interneuron network (P-I) gamma oscillations
Rationale for this assumption is given by the facts that area CA1 and the directly interconnected subiculum send excitatory projections to the PrC and that pyramidal cells persistently fire in a synchronized rhythmic manner during P-I oscillations (Tiesinga and Sejnowski, 2009; ter Wal and Sejnowski, 2014)
Summary
There is overwhelming evidence that several cognitive functions in mammals require theta (4–12 Hz) and/or gamma (30–80 Hz) network oscillations in the hippocampus and associated rhinal cortices, including the perirhinal cortex (PrC; Zola-Morgan et al, 1993; Bilkey and Heinemann, 1999; Fell et al, 2001; Colgin and Moser, 2010; Buzsáki and Wang, 2012). Two experimentally induced types of this self-produced rhythmicity (and most likely natural CA1 gamma oscillations) involve feedback inhibition of pyramidal neurons (Whittington et al, 1997; Buzsáki and Wang, 2012; Pietersen et al, 2014), but it remains unclear whether area CA1 harbors the circuitry for a generation of prototypic pyramidal-interneuron network (P-I) gamma oscillations Such oscillations must exclusively arise from sustained suprathreshold depolarization and feedback inhibition of pyramidal cells (Bartos et al, 2007; Tiesinga and Sejnowski, 2009; ter Wal and Sejnowski, 2014), without direct excitatory effects of the induction agents/techniques on the mediating GABAergic interneurons (cf., Whittington et al, 1997; Pietersen et al, 2014; Yi et al, 2014), and could impact network oscillations in the PrC (Bilkey and Heinemann, 1999; Fell et al, 2001). We performed different types of electrophysiological measurements in acute brain slices and slightly anesthetized animals and combined them with sustained local ChR2 activation in dorsal area CA1
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