Long-term population spike-timing-dependent plasticity promotes synaptic tagging but not cross-tagging in rat hippocampal area CA1

Mar 2, 2019Proceedings of the National Academy of Sciences of the United States of America

Long-lasting timing-based synaptic changes help mark active connections but do not spread this marking to others in the memory area of rat brains

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Abstract

The potentiation of synaptic activity in CA1 neurons lasted for 4 hours after specific pre- and postsynaptic pairings.

Synaptic plasticity was influenced by the timing and order of pre- and postsynaptic activities.
The strongest and most enduring synaptic potentiation occurred when presynaptic activity coincided with or preceded postsynaptic activity.
When postsynaptic activity preceded presynaptic stimulation by 20 ms, initial synaptic enhancement turned into depression over time.
Pairing pre- and postsynaptic activities reduced the number of events needed to induce synaptic changes, mimicking effects seen with repeated stimulation.
pSTDP may play a significant role in determining synaptic strength in the hippocampal CA3-CA1 circuit.

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In spike-timing-dependent plasticity (STDP), the direction and degree of synaptic modification are determined by the coherence of pre- and postsynaptic activities within a neuron. However, in the adult rat hippocampus, it remains unclear whether STDP-like mechanisms in a neuronal population induce synaptic potentiation of a long duration. Thus, we asked whether the magnitude and maintenance of synaptic plasticity in a population of CA1 neurons differ as a function of the temporal order and interval between pre- and postsynaptic activities. Modulation of the relative timing of Schaffer collateral fibers (presynaptic component) and CA1 axons (postsynaptic component) stimulations resulted in an asymmetric population STDP (pSTDP). The resulting potentiation in response to 20 pairings at 1 Hz was largest in magnitude and most persistent (4 h) when presynaptic activity coincided with or preceded postsynaptic activity. Interestingly, when postsynaptic activation preceded presynaptic stimulation by 20 ms, an immediate increase in field excitatory postsynaptic potentials was observed, but it eventually transformed into a synaptic depression. Furthermore, pSTDP engaged in selective forms of late-associative activity: It facilitated the maintenance of tetanization-induced early long-term potentiation (LTP) in neighboring synapses but not early long-term depression, reflecting possible mechanistic differences with classical tetanization-induced LTP. The data demonstrate that a pairing of pre- and postsynaptic activities in a neuronal population can greatly reduce the required number of synaptic plasticity-evoking events and induce a potentiation of a degree and duration similar to that with repeated tetanization. Thus, pSTDP determines synaptic efficacy in the hippocampal CA3-CA1 circuit and could bias the CA1 neuronal population toward potentiation in future events.

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Long-term population spike-timing-dependent plasticity promotes synaptic tagging but not cross-tagging in rat hippocampal area CA1

Abstract

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