Novelty-Induced Phase-Locked Firing to Slow Gamma Oscillations in the Hippocampus: Requirement of Synaptic Plasticity

Abstract

Temporally precise neuronal firing phase-locked to gamma oscillations is thought to mediate the dynamic interaction of neuronal populations, which is essential for information processing underlying higher-order functions such as learning and memory. However, the cellular mechanisms determining phase locking remain unclear. By devising a virus-mediated approach to perform multi-tetrode recording from genetically manipulated neurons, we demonstrated that synaptic plasticity dependent on the GluR1 subunit of AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole propionate) receptor mediates two dynamic changes in neuronal firing in the hippocampal CA1 area during novel experiences: the establishment of phase-locked firing to slow gamma oscillations and the rapid formation of the spatial firing pattern of place cells. The results suggest a series of events potentially underlying the acquisition of new spatial information: slow gamma oscillations, originating from the CA3 area, induce the two GluR1-dependent changes of CA1 neuronal firing, which in turn determine information flow in the hippocampal-entorhinal system.

Methodological standards and interpretation of video‐electroencephalography in adult control rodents. A TASK1‐WG1 report of theAES/ILAETranslational Task Force of the ILAE

“…For example, during exploratory behavior (Fig. A), an increase of specific frequency bands (theta and gamma oscillations) was observed . In addition, hippocampal theta power was decreased in rats placed in a novel environment .…”

“…3A), an increase of specific frequency bands (theta and gamma oscillations) was observed. 42 In addition, hippocampal theta power was decreased in rats placed in a novel environment. 43 If the behavioral state of the animal changes but the EEG does not, it is worth considering the possibility that there is a recording problem.…”

Rhythms of the hippocampal network

“…Specifically, some studies have described novelty-related increases in slow gamma in rats 125,160,161 . One possible explanation for these observations is that slow gamma promotes interactions between CA3 and CA1 in general, and that these interactions are heightened when the animal is in novel environments.…”

Beta2 oscillations in the hippocampal-cortical novelty detection circuit

“…We and others have identified beta2 as an oscillatory feature in novelty detection in the HC (Berke et al, 2008;França et al, 2014;Kitanishi et al, 2015). This oscillation has a spectral peak around 20 to 30Hz in mice (Berke et al, 2008;França et al, 2014), and slightly faster in rats -25 to 48Hz (Kitanishi et al, 2015).…”

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Novelty detection is a core feature of behavioral adaptation, and involves cascades of neuronal responsesfrom initial evaluation of the stimulus to the encoding of new representations -resulting in the behavioral ability to respond to an unexpected input (Kafkas and Montaldi, 2018;van Kesteren et al, 2012). In the past decade, a new important novelty detection feature, beta2 (~20 -30 Hz) oscillations, has been described in the hippocampus (Berke et al, 2008;França et al, 2014;Kitanishi et al, 2015). However, the interactions between beta2 and the hippocampal network is unknown, as well as the role -or even the presence -of beta2 in other areas involved with novelty detection.

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