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Cited by 966Neural dynamics and brain functionMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat

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Csicsvari, Jozsef, Hirase, Hajime, Czurkó, András, Mamiya, Akira, Buzsáki, György·1999·The Journal of Neuroscience
DOI 10.1523/jneurosci.19-01-00274.1999PMC PMC6782375
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Abstract

We examined whether excitation and inhibition are balanced in hippocampal cortical networks. Extracellular field and single-unit activity were recorded by multiple tetrodes and multisite silicon probes to reveal the timing of the activity of hippocampal CA1 pyramidal cells and classes of interneurons during theta waves and sharp wave burst (SPW)-associated field ripples. The somatic and dendritic inhibition of pyramidal cells was deduced from the activity of interneurons in the pyramidal layer [int(p)] and in the alveus and st. oriens [int(a/o)], respectively. Int(p) and int(a/o) discharged an average of 60 and 20 degrees before the population discharge of pyramidal cells during the theta cycle, respectively. SPW ripples were associated with a 2.5-fold net increase of excitation. The discharge frequency of int(a/o) increased, decreased ("anti-SPW" cells), or did not change ("SPW-independent" cells) during SPW, suggesting that not all interneurons are innervated by pyramidal cells. Int(p) either fired together with (unimodal cells) or both before and after (bimodal cells) the pyramidal cell burst. During fast-ripple oscillation, the activity of interneurons in both the int(p) and int(a/o) groups lagged the maximum discharge probability of pyramidal neurons by 1-2 msec. Network state changes, as reflected by field activity, covaried with changes in the spike train dynamics of single cells and their interactions. Summed activity of parallel-recorded interneurons, but not of pyramidal cells, reliably predicted theta cycles, whereas the reverse was true for the ripple cycles of SPWs. We suggest that network-driven excitability changes provide temporal windows of opportunity for single pyramidal cells to suppress, enable, or facilitate selective synaptic inputs.

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  • SW-Rs occur mainly during SWS but also during nonexploratory wakefulness.

    “SW-Rs occur mainly during SWS but also during nonexploratory wakefulness (e.g., drinking, grooming, and quiet wakefulness).”

    From About Sleep's Role in Memory (2013) · cites this paper as [241]

    The introductory passage (page unavailable) associates sharp waves and fast oscillations with slow-wave sleep, immobility, and consummatory behaviors, supporting occurrence during sleep and nonexploratory wakefulness. It does not establish that SW-Rs occur mainly during slow-wave sleep or specifically name drinking and grooming. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • SW-Rs may conversely promote LTP and spike time-dependent plasticity in hippocampal circuits.

    “SW-Rs may conversely promote LTP and spike timedependent plasticity in hippocampal circuits (97,159,241,640,777).”

    From About Sleep's Role in Memory (2013) · cites this paper as [241]

    In “SPW and ripples: physiological implications” (page unavailable), the paper proposes that SPW-associated bursts may produce plastic changes at downstream synapses and that dendritic bursts may change active synapses locally. It does not identify those changes specifically as LTP or spike time-dependent plasticity. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Proper Bayesian inference in complex state spaces would require extensive computation time, creating a fundamental temporal mismatch with the brain's millisecond responses.

    “The brain must respond to environmental challenges within milliseconds, while proper Bayesian inference in complex state spaces would require extensive computation time, creating a fundamental temporal mismatch (Csicsvari et al. 1999; Hari and Parkkonen 2015).”

    From The myth of the Bayesian brain (2025) · cites this paper as Csicsvari et al. 1999

    The Discussion describes millisecond-scale spike timing and temporal coding, but does not discuss Bayesian inference or a mismatch between its computational demands and brain response times. Searches for Bayesian inference, complex state spaces, and computational time returned no passage addressing that claim. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

  • About 250,000 principal cells from ipsilateral ECIII synapse onto the CA1 region, and approximately 2% of these cells are active per theta cycle at a low firing rate, so ECIII cells could provide 5000 input spikes to ipsilateral CA1.

    “About 250,000 principal cells from ipsilateral ECIII synapse onto the CA1 region (Andersen et al., 2006), and approximately 2% of these cells are active per theta cycle at a low firing rate (Csicsvari et al., 1999; Mizuseki et al., 2009). Therefore, ECIII cells could provide 5000 input spikes to ipsilateral CA1 (Equation 3).”

    From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Csicsvari et al., 1999

  • Units were deemed independent from each other by their distinct spike waveform, the absence of refractory period in their cross-correlations and separable principal component boundaries using a measure based on the Mahalanobis distance.

    “Units were deemed independent from each other by i) their distinct spike waveform, ii) the absence of refractory period in their cross-correlations and iii) separable principal component boundaries using a measure based on the Mahalanobis distance24,26.”

    From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [24]

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Authors
Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A., & Buzsáki, G.
Affiliations
Rutgers, The State University of New Jersey (US)
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
1999-01-01
Volume
19
Issue
1
Pages
274-287
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.19-01-00274.1999
PMC
PMC6782375
OpenAlex
W2099512174
Cited by
966
References
67
Citations by year
2026: 19 · 2025: 40 · 2024: 26 · 2023: 35 · 2022: 42 · 2021: 36 · 2020: 51 · 2019: 59 · 2018: 36 · 2017: 43 · 2016: 40 · 2015: 41 · 2014: 51 · 2013: 49 · 2012: 46
FWCI
13.20
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (5p41rr009754-09, 1P41RR09754)
  • National Institute of Mental Health (R01MH054671, MH54671)
  • National Institute of Neurological Disorders and Stroke (R01NS034994, NS-34994)
  • National Center for Research Resources (1P41RR-09754)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
hippocampus, CA1 pyramidal neurons, interneurons, theta oscillations, sharp-wave ripples, fast ripples, excitation-inhibition balance, oscillatory coupling, network state, alveoli
MeSH terms
Animals, Behavior, Animal, Interneurons, Male, Nerve Net, Oscillometry, Theta Rhythm, Linear Models, Pyramidal Cells, Rats

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