Abstract
BackgroundTheta rhythm in the hippocampal formation is a main feature of exploratory behaviour and is believed to enable the encoding of new spatial information and the modification of synaptic weights. Cyclic changes of dentate gyrus excitability during theta rhythm are related to its function, but whether theta epochs per se are able to alter network properties of dentate gyrus for long time-periods is still poorly understood.Methodology/Principal FindingsWe used low-frequency stimulation protocols that amplify the power of endogenous theta oscillations, in order to estimate the plasticity effect of endogenous theta oscillations on a population level. We found that stimulation-induced augmentation of the theta rhythm is linked to a subsequent increase of neuronal excitability and decrease of the synaptic response. This EPSP-to-Spike uncoupling is related to an increased postsynaptic spiking on the positive phases of theta frequency oscillations. Parallel increase of the field EPSP slope and the population spike occurs only after concurrent pre- and postsynaptic activation. Furthermore, we observed that long-term potentiation (>24 h) occurs in the dentate gyrus of freely behaving adult rats after phasic activity of entorhinal afferents in the theta-frequency range. This plasticity is proportional to the field bursting activity of granule cells during the stimulation, and may comprise a key step in spatial information transfer. Long-term potentiation of the synaptic component occurs only when the afferent stimulus precedes the evoked population burst, and is input-specific.Conclusions/SignificanceOur data confirm the role of the dentate gyrus in filtering information to the subsequent network during the activated state of the hippocampus.
Highlights
In an effort to more closely approximate endogenous conditions for information storage in the hippocampus, many studies have addressed the relationship between synaptic plasticity and neuronal oscillations during exploratory behaviour
We examined the possibility that dentate gyrus granule cells may change their firing patterns proportionally to the preceding spiking activity in order to enable synaptic information storage
By comparing the synaptic changes of the neuronal populations that underwent certain firing patterns to those that were not affected by the stimulation, we were able to link the local field oscillations with subsequent synaptic plasticity
Summary
In an effort to more closely approximate endogenous conditions for information storage in the hippocampus, many studies have addressed the relationship between synaptic plasticity and neuronal oscillations during exploratory behaviour. Long-term potentiation (LTP) of synaptic strength is widely supported as a spatial memory mechanism. Field potential oscillations at theta frequency (5–12 Hz) are believed critical for the acquisition of new information by active hippocampal ensembles [1], and are a typical feature of network activity during novel spatial exploration. Modification of synaptic weights happens very fast during the activated state of the hippocampus [2], with entorhinal-hippocampal network oscillations at theta frequency playing a crucial role in this process [3]. Theta rhythm in the hippocampal formation is a main feature of exploratory behaviour and is believed to enable the encoding of new spatial information and the modification of synaptic weights. Cyclic changes of dentate gyrus excitability during theta rhythm are related to its function, but whether theta epochs per se are able to alter network properties of dentate gyrus for long time-periods is still poorly understood
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