Relationship of hippocampal theta and gamma oscillations to potentiation of synaptic transmission

Abstract

In the hippocampus in vivo, both synaptic plasticity and network activity are closely interdependent. We have found that immediately after an attempt to induce long-term potentiation (LTP), changes in theta (5-10 Hz) and gamma (30-100 Hz) activity correlate tightly with the occurrence of LTP, suggesting that tetanisation-driven activation of sensory inputs synchronises the activity of granule cells and interneurons, and thus, facilitates the encoding of acquired stimuli. This results in increase of theta and gamma power, and elevates the probability that afferent stimuli both coincide with the peak of theta cycle and reach their post-synaptic target within the gamma time-window (of 10-30 ms). Both these mechanisms can effectively shift the direction, of tetanisation-induced changes in synaptic weight, towards potentiation and induction of LTP. Here, we discuss our findings in the context of possible mechanisms that link theta and gamma oscillations with LTP induction, as well as their role in information processing and formation of memories.

Keywords: LTP; gamma; in vivo; network activity; oscillations; synaptic plasticity; tetanisation; theta.

Figure 1

Transient enhancement of theta and gamma power in the post-tetanisation period correlates with potentiation of synaptic transmission in the dentate gyrus of freely moving rats. (A) Examples of EEG epochs, which comprise 100 s long periods of tetanisation (200 Hz, 10 trains: first train is marked by arrow) and following 300 s, recorded in rats that showed either LTP (left panel), STP (middle panel) or failure of potentiation (right panel), respectively. Asterisk denotes the period immediately after HFT, when the amplitude of network oscillations is higher in LTP and STP cases, in comparison with failed potentiation. Scale bar: 20 s. (B) Successful potentiation (LTP and STP) of synaptic transmission is associated with a prominent increase of the relative theta and gamma power particularly in the period encompassing 100 s after tetanisation. The results were pooled for LTP, STP and failure groups and presented as Mean ± S.E.M. (modified from Bikbaev and Manahan-Vaughan, 2007).

Figure 2

A schematic representation of the consequences of high-frequency tetanisation that occur on the network and cellular levels, and lead towards long-term potentiation of synaptic transmission. (A) Strong afferent stimulation results in an enhancement of both theta and gamma oscillations, which occurs within 5 min interval after tetanisation and can be mediated via GABARs, NMDARs and mGluRs. (B) Tetanisation-triggered activation of both ionotropic and metabotropic glutamate receptors is followed by the expression of plasticity-related immediate-early genes (IEGs) and protein synthesis, which can underlie structural synaptic reorganisation and long-term increase in synaptic efficacy. Experimental procedures that inhibit the induction, expression or maintenance of LTP can result in impairment of post-tetanic potentiation, STP, early LTP or late LTP (1–4, respectively). Grey arrows denote possible links between NMDAR and mGluR activation and facilitation of network activity in theta and gamma frequency bands.