Muscarinic blockade weakens interaction of gamma with theta rhythms in mouse hippocampus

Abstract

theta (4-12 Hz) and gamma (40-90) oscillations are prominent rhythms in the mammalian brain. A striking feature of these rhythms, possibly vital to memory encoding, is their specific coordination in a manner that has been termed 'nesting', i.e. the preferred occurrence of bouts of gamma activity during specific phases of theta. Both rhythms are shaped by the neuromodulator acetylcholine, but it is unknown to what degree their coordination is influenced by cholinergic neuromodulation. Here, we investigated the effects of a blockade of muscarinic acetylcholine receptors by atropine on theta and gamma oscillations, and their interaction, in mouse hippocampus in vivo. Multi-site recordings from area CA1 of freely moving mice showed that under control conditions gamma activity was amplitude-modulated at theta frequencies. This coordination of theta and gamma oscillations, as assessed by cross-correlation of theta with the gamma envelope, was prominent in basal and apical dendritic laminae but not in intermediate laminae. It was stronger during active exploration than during awake immobility. Atropine (50 mg/kg intraperitoneal) altered several aspects of the individual and nested rhythms. It rendered theta activity irregular, decreased theta oscillation frequency and reduced gamma power. Atropine also reduced the amplitude-modulation of gamma oscillations at theta frequencies, in part by perturbing the coordination of the rhythms on a short time scale. Thus, our findings demonstrate that phase locking of the amplitude of gamma oscillations to theta in hippocampal area CA1 is partially governed by neuronal elements harbouring muscarinic receptors.

Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons

“…Our results show that mutual inhibition is dispensable for in vivo gamma oscillations and stress the importance of recurrent excitation and feed-back inhibition (9). In all mammals examined, including humans, gamma oscillations are modulated by concurrent theta rhythm (6)(7)(8)(9)(10)50). This thetagamma coupling may serve as a general coding scheme that coordinates distributed cortical areas, encodes serial information and working memory, and aids theta phase precession of place cells (5,(10)(11)(12)(13)(14)21).…”

Altered GABAA,slowInhibition and Network Oscillations in Mice Lacking the GABAAReceptor β3Subunit

“…Field potentials from area CA1 of the dorsal hippocampus were recorded as described previously (Hentschke et al 2007). Briefly, under isoflurane anesthesia, the animals were chronically implanted with 16-channel linear microwire arrays (Jellema and Weijnen 1991).…”

Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task

“…Among brain rhythms, theta oscillations in local field potentials (LFPs) recorded in the hippocampus are prominent during active behaviors (2)(3)(4)(5), and these have long been intensively analyzed in the rodent in relation to spatial navigation (6), memory (7), and sleep (8). Theta-band rhythms (4)(5)(6)(7)(8)(9)(10)(11)(12) are now known to occur in other cortical (9)(10)(11)(12) and subcortical (12)(13)(14)(15) regions, however, including the striatum (14)(15)(16)(17), studied here. Gamma oscillations (30-100 Hz) have also received special attention because of their proposed role in functions such as sensory binding (18), selective attention (19)(20)(21), transient neuronal assembly formation (22), and information transmission and storage (23)(24)(25).…”

“…In one type of interaction, the phase of low-frequency rhythms modulates the amplitude of higher-frequency oscillations (9,10,30). For example, theta phase is known to modulate gamma power in rodent hippocampal and cortical circuits (2)(3)(4)31), and the phase of theta rhythms recorded in the human neocortex can modulate wide-band (60-200 Hz) high-frequency oscillations (10). Such theta-gamma nesting is thought to play a role in sequential memory organization and maintenance of working memory, and more generally in ''phase coding'' (25,31).…”