Journal Article

Cell-specific synaptic plasticity induced by network oscillations

Zarnadze, Shota, Geiger, Jörg RP, Gloveli, Tengis, Schmitz, Dietmar, Bäuerle, Peter, Dugladze, Tamar, Santos-Torres, Julio, Böhm, Claudia

2016

Overview

Gamma rhythms are known to contribute to the process of memory encoding. However, little is known about the underlying mechanisms at the molecular, cellular and network levels. Using local field potential recording in awake behaving mice and concomitant field potential and whole-cell recordings in slice preparations we found that gamma rhythms lead to activity-dependent modification of hippocampal networks, including alterations in sharp wave-ripple complexes. Network plasticity, expressed as long-lasting increases in sharp wave-associated synaptic currents, exhibits enhanced excitatory synaptic strength in pyramidal cells that is induced postsynaptically and depends on metabotropic glutamate receptor-5 activation. In sharp contrast, alteration of inhibitory synaptic strength is independent of postsynaptic activation and less pronounced. Further, we found a cell type-specific, directionally biased synaptic plasticity of two major types of GABAergic cells, parvalbumin- and cholecystokinin-expressing interneurons. Thus, we propose that gamma frequency oscillations represent a network state that introduces long-lasting synaptic plasticity in a cell-specific manner. Changes in the strength of synapses – the connections between neurons – form the basis of learning and memory. This process, which is known as synaptic plasticity, incorporates transient experiences into persistent memory traces. However, a single synapse should not be viewed in isolation. Neurons typically belong to extensive networks made up of large numbers of cells, which show coordinated patterns of activity. The synchronized firing of the neurons in such a network is referred to as a network oscillation. The frequency of an oscillation – that is, the number of times per second that its component cells are active at the same time – reflects distinct physiological functions. For example, high frequency oscillations called gamma waves help new memories to form, but it is not clear exactly how they do this. By studying gamma oscillations in a brain region called the hippocampus, Zarnadze, Bäuerle et al. provide insights into the underlying mechanisms. Signals from “excitatory” neurons make the neuron on the other side of the synapse more likely to fire in response, and signals for “inhibitory” neurons make it less likely to fire. By recording the activity of excitatory neurons in mouse brain slices, Zarnadze, Bäuerle et al. show that gamma oscillations increase the strength of excitatory synapses in the hippocampus, allowing neurons to signal more easily across these connections. Blocking the activity of a protein called metabotropic glutamate receptor 5 prevents this increase in excitatory synaptic strength, suggesting that these receptors play an important role in memory processing. In contrast to excitatory neurons, gamma oscillations have different effects on two types of inhibitory neurons within the hippocampus. The oscillations increase the excitability of gamma-supporting inhibitory neurons, but at the same time reduce that of gamma-disturbing inhibitory neurons. These opposing changes in turn support synaptic plasticity. By showing that gamma oscillations contribute to changes in synaptic strength within the hippocampus, Zarnadze, Bäuerle et al. help to explain the importance of these rhythms for memory processing. Further research is now needed to fully decipher the roles of different cell types, and the synaptic connections between them, in the formation of new memories.

• Publisher: eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Cholecystokinin / Cholecystokinin - genetics / Cholecystokinin - metabolism / Electrophysiological recording / Excitatory Postsynaptic Potentials - physiology / GABAergic Neurons - cytology / GABAergic Neurons - metabolism / Gamma Rhythm - physiology / gamma rhythms / Gene Expression / Glutamic acid receptors (metabotropic) / Hippocampal plasticity / Hippocampus / Hippocampus - cytology / Hippocampus - metabolism / Immunoglobulins / interneuron / Interneurons / Interneurons - cytology / Interneurons - metabolism / Laboratories / Memory / mGluR5 / Mice / Mice, Inbred C57BL / Nerve Net - metabolism / Nerve Net - ultrastructure / Neural circuitry / Neuronal Plasticity - physiology / Neuroplasticity / Neuroscience / Neurosciences / Observations / Organ Specificity / Oscillations / Parvalbumin / Parvalbumins - genetics / Parvalbumins - metabolism / patch-clamp methodology / Patch-Clamp Techniques / Physiological aspects / Pyramidal cells / Pyramidal Cells - cytology / Pyramidal Cells - metabolism / Receptor, Metabotropic Glutamate 5 - genetics / Receptor, Metabotropic Glutamate 5 - metabolism / sharp wave ripples / Synaptic plasticity / Synaptic strength / Synaptic Transmission - physiology / Wavelet transforms / γ-Aminobutyric acid