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A developmental increase of inhibition promotes the emergence of hippocampal ripples

Author

Listed:
  • Irina Pochinok

    (University Medical Center Hamburg-Eppendorf)

  • Tristan M. Stöber

    (Frankfurt Institute for Advanced Studies)

  • Jochen Triesch

    (Frankfurt Institute for Advanced Studies)

  • Mattia Chini

    (University Medical Center Hamburg-Eppendorf)

  • Ileana L. Hanganu-Opatz

    (University Medical Center Hamburg-Eppendorf)

Abstract

Sharp wave-ripples (SPW-Rs) are a hippocampal network phenomenon critical for memory consolidation and planning. SPW-Rs have been extensively studied in the adult brain, yet their developmental trajectory is poorly understood. While SPWs have been recorded in rodents shortly after birth, the time point and mechanisms of ripple emergence are still unclear. Here, we combine in vivo electrophysiology with optogenetics and chemogenetics in 4 to 12-day-old mice to address this knowledge gap. We show that ripples are robustly detected and induced by light stimulation of channelrhodopsin-2-transfected CA1 pyramidal neurons only from postnatal day 10 onwards. Leveraging a spiking neural network model, we mechanistically link the maturation of inhibition and ripple emergence. We corroborate these findings by reducing ripple rate upon chemogenetic silencing of CA1 interneurons. Finally, we show that early SPW-Rs elicit a more robust prefrontal cortex response than SPWs lacking ripples. Thus, development of inhibition promotes ripples emergence.

Suggested Citation

  • Irina Pochinok & Tristan M. Stöber & Jochen Triesch & Mattia Chini & Ileana L. Hanganu-Opatz, 2024. "A developmental increase of inhibition promotes the emergence of hippocampal ripples," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44983-z
    DOI: 10.1038/s41467-024-44983-z
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    References listed on IDEAS

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    1. Anja L. Dorrn & Kexin Yuan & Alison J. Barker & Christoph E. Schreiner & Robert C. Froemke, 2010. "Developmental sensory experience balances cortical excitation and inhibition," Nature, Nature, vol. 465(7300), pages 932-936, June.
    2. Anli A. Liu & Simon Henin & Saman Abbaspoor & Anatol Bragin & Elizabeth A. Buffalo & Jordan S. Farrell & David J. Foster & Loren M. Frank & Tamara Gedankien & Jean Gotman & Jennifer A. Guidera & Kari , 2022. "A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Torfi Sigurdsson & Kimberly L. Stark & Maria Karayiorgou & Joseph A. Gogos & Joshua A. Gordon, 2010. "Impaired hippocampal–prefrontal synchrony in a genetic mouse model of schizophrenia," Nature, Nature, vol. 464(7289), pages 763-767, April.
    4. Asako Noguchi & Roman Huszár & Shota Morikawa & György Buzsáki & Yuji Ikegaya, 2022. "Inhibition allocates spikes during hippocampal ripples," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
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