期刊
JOURNAL OF NEUROSCIENCE
卷 38, 期 12, 页码 3124-3146出版社
SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.0188-17.2018
关键词
basket cells; CA1; fast gamma; memory consolidation; network oscillations; sharp wave/ripple complexes
资金
- Bundesministerium fur Bildung und Forschung (Bernstein Center for Computational Neuroscience Berlin Grant) [01GQ1001A]
- Bundesministerium fur Bildung und Forschung (Bernstein Focus Neuronal Foundations of Learning Grant) [01GQ0972]
- Deutsche Forschungsgemeinschaft [GRK1589, SFB958, KE788/3-1]
- NeuroCure excellence cluster
- Einstein Center for Neurosciences Berlin
Hippocampal ripples are involved in memory consolidation, but the mechanisms underlying their generation remain unclear. Models relying on interneuron networks in the CA1 region disagree on the predominant source of excitation to interneurons: either direct, via the Schaffer collaterals that provide feedforward input from CA3 to CA1, or indirect, via the local pyramidal cells in CA1, which are embedded in a recurrent excitatory-inhibitory network. Here, we used physiologically constrained computational models of basket-cell networks to investigate how they respond to different conditions of transient, noisy excitation. We found that direct excitation of interneurons could evoke ripples (140 - 220 Hz) that exhibited intraripple frequency accommodation and were frequency-insensitive to GABA modulators, as previously shown in in vitro experiments. In addition, the indirect excitation of the basket-cell network enabled the expression of intraripple frequency accommodation in the fast-gamma range (90 - 140 Hz), as in vivo. In our model, intraripple frequency accommodation results from a hysteresis phenomenon in which the frequency responds differentially to the rising and descending phases of the transient excitation. Such a phenomenon predicts a maximum oscillation frequency occurring several milliseconds before the peak of excitation. We confirmed this prediction for ripples in brain slices from male mice. These results suggest that ripple and fast-gamma episodes are produced by the same interneuron network that is recruited via different excitatory input pathways, which could be supported by the previously reported intralaminar connectivity bias between basket cells and functionally distinct subpopulations of pyramidal cells in CA1. Together, our findings unify competing inhibition-first models of rhythm generation in the hippocampus.
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