Abstract
Long-term potentiation (LTP) is commonly used to study synaptic plasticity but the associated changes in the spontaneous activity of individual neurons or the computational properties of neural networks in vivo remain largely unclear. The multisynaptic origin of spontaneous spikes makes it difficult to estimate the impact of a particular potentiated input. Accordingly, we adopted an approach that isolates pathway-specific postsynaptic activity from raw local field potentials (LFPs) in the rat hippocampus in order to study the effects of LTP on ongoing spike transfer between cell pairs in the CA3-CA1 pathway. CA1 Schaffer-specific LFPs elicited by spontaneous clustered firing of CA3 pyramidal cells involved a regular succession of elementary micro-field-EPSPs (gamma-frequency) that fired spikes in CA1 units. LTP increased the amplitude but not the frequency of these ongoing excitatory quanta. Also, the proportion of Schaffer-driven spikes in both CA1 pyramidal cells and interneurons increased in a cell-specific manner only in previously connected CA3-CA1 cell pairs, i.e., when the CA3 pyramidal cell had shown pre-LTP significant correlation with firing of a CA1 unit and potentiated spike-triggered average (STA) of Schaffer LFPs following LTP. Moreover, LTP produced subtle reorganization of presynaptic CA3 cell assemblies. These findings show effective enhancement of pathway-specific ongoing activity which leads to increased spike transfer in potentiated segments of a network. They indicate that plastic phenomena induced by external protocols may intensify spontaneous information flow across specific channels as proposed in transsynaptic propagation of plasticity and synfire chain hypotheses that may be the substrate for different types of memory involving multiple brain structures.
Highlights
The information flow between brain nuclei is made through synchronous activity in rapidly changing neuron combinations or cell assemblies (Stevens and Zador, 1998; Kumar et al, 2010)
local field potentials (LFPs) generators can be considered as dual entities, formed by one homogenous presynaptic population and the subcellular domain to which their axons project onto target neurons
Each is characterized by a constant spatial distribution and a temporal activation varying for different LFP segments (Korovaichuk et al, 2010; Makarova et al, 2011)
Summary
The information flow between brain nuclei is made through synchronous activity in rapidly changing neuron combinations or cell assemblies (Stevens and Zador, 1998; Kumar et al, 2010). Such flow can be modulated by synaptic plasticity, a crucial mechanism in basic cognitive processes such as memory, learning, and adaptation (Martin et al, 2000; Lynch, 2004; Kandel, 2009). From the mechanistic point of view, it is difficult to relate behavioral and cognitive functions requiring long lasting changes in neural substrates with plastic phenomena induced by experimental protocols of repetitive activation in small segments of a network. Spikes produced by any individual neuron may have a multisynaptic origin, complicating the correlation of ongoing changes in spike series with specific variations of incoming activity in one or another presynaptic population
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