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Proc Natl Acad Sci U S A. 2019 Mar 19;116(12):5737-5746. doi: 10.1073/pnas.1817643116. Epub 2019 Feb 28.

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

Author information

1
Department of Physiology, National University of Singapore, Singapore 117593.
2
Neurobiology/Aging Programme, Life Sciences Institute, Centre for Life Sciences, National University of Singapore, Singapore 117456.
3
Department of Biomedical Engineering, City College of New York, New York, NY 10031.
4
Institutes of Brain Science, State Key Laboratory of Medical Neurobiology, Ministry of Education Frontiers Centre for Brain Science, Fudan University, Shanghai 200032, People's Republic of China behnish@fudan.edu.cn phssks@nus.edu.sg.
5
Department of Physiology, National University of Singapore, Singapore 117593; behnish@fudan.edu.cn phssks@nus.edu.sg.

Abstract

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.

KEYWORDS:

STDP; area CA1; synaptic capture; synaptic plasticity; synaptic tagging

PMID:
30819889
PMCID:
PMC6431168
[Available on 2019-09-19]
DOI:
10.1073/pnas.1817643116

Conflict of interest statement

The authors declare no conflict of interest.

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