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Hippocampal CA1 Ripples as Inhibitory Transients.

Malerba P, Krishnan GP, Fellous JM, Bazhenov M - PLoS Comput. Biol. (2016)

Bottom Line: Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep.We found that noise-induced loss of synchrony among CA1 interneurons dynamically constrains individual ripple duration.Our study proposes a novel mechanism of hippocampal ripple generation consistent with a broad range of experimental data, and highlights the role of noise in regulating the duration of input-driven oscillatory spiking in an inhibitory network.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology and Neuroscience, University of California Riverside, Riverside, California, United States of America.

ABSTRACT
Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep. Neurons active during behavior reactivate in both structures during sleep, in conjunction with characteristic brain oscillations that may form the neural substrate of memory consolidation. In the hippocampus, replay occurs within sharp wave-ripples: short bouts of high-frequency activity in area CA1 caused by excitatory activation from area CA3. In this work, we develop a computational model of ripple generation, motivated by in vivo rat data showing that ripples have a broad frequency distribution, exponential inter-arrival times and yet highly non-variable durations. Our study predicts that ripples are not persistent oscillations but result from a transient network behavior, induced by input from CA3, in which the high frequency synchronous firing of perisomatic interneurons does not depend on the time scale of synaptic inhibition. We found that noise-induced loss of synchrony among CA1 interneurons dynamically constrains individual ripple duration. Our study proposes a novel mechanism of hippocampal ripple generation consistent with a broad range of experimental data, and highlights the role of noise in regulating the duration of input-driven oscillatory spiking in an inhibitory network.

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CA1 ripples have standardized durations.From a 25hr experiment recording, ripples are identified as large amplitude excursion of the band-passed LFP. (a) The leftmost plots show wide band (1-400Hz) LFP recordings from CA1. The rightmost plots show the same LFPs band-pass filtered between 50Hz and 350Hz. (b) Histogram of ripple frequencies (count normalized to total number of ripples). The blue line is its Gaussian distribution fit. (c) Histogram of ripple inter-arrival times, and exponential fit in red. (d) Histogram of ripple durations, showing a high kurtosis, hence highlighting that ripples are very different in frequency and have almost memory-less arrival times, but their duration has small variability.
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pcbi.1004880.g001: CA1 ripples have standardized durations.From a 25hr experiment recording, ripples are identified as large amplitude excursion of the band-passed LFP. (a) The leftmost plots show wide band (1-400Hz) LFP recordings from CA1. The rightmost plots show the same LFPs band-pass filtered between 50Hz and 350Hz. (b) Histogram of ripple frequencies (count normalized to total number of ripples). The blue line is its Gaussian distribution fit. (c) Histogram of ripple inter-arrival times, and exponential fit in red. (d) Histogram of ripple durations, showing a high kurtosis, hence highlighting that ripples are very different in frequency and have almost memory-less arrival times, but their duration has small variability.

Mentions: We started investigating the nature of ripple oscillations by studying LFP recordings in hippocampal CA1 in rats. Representative examples of the wide-band and band-passed recordings are shown in Fig 1A. We focused on a few salient characteristics of ripple waves, such as frequency, duration and inter-arrival time (defined as the time between a ripple event and the next). Fig 1 shows that ripple frequency, defined as the inverse of the average inter-peak interval during a ripple event, was normally distributed around 163.5 (± 20.6) Hz (Fig 1B), their inter-arrival times were approximately exponential, with fitted rate 1.7748 Hz (Fig 1C), and their duration (Fig 1C) was centered about 51 (± 9.4) ms showing a high-kurtosis distribution (K = 20.1952, where for a normal distribution K = 3) [28]. Note that ripple frequency is representative of the peak-to-peak time within a given ripple (see S1 Fig for a representation), while the count of ripple events in a given time interval would be called ripple density, and can be found as the inverse of the inter-arrival times in such interval.


Hippocampal CA1 Ripples as Inhibitory Transients.

Malerba P, Krishnan GP, Fellous JM, Bazhenov M - PLoS Comput. Biol. (2016)

CA1 ripples have standardized durations.From a 25hr experiment recording, ripples are identified as large amplitude excursion of the band-passed LFP. (a) The leftmost plots show wide band (1-400Hz) LFP recordings from CA1. The rightmost plots show the same LFPs band-pass filtered between 50Hz and 350Hz. (b) Histogram of ripple frequencies (count normalized to total number of ripples). The blue line is its Gaussian distribution fit. (c) Histogram of ripple inter-arrival times, and exponential fit in red. (d) Histogram of ripple durations, showing a high kurtosis, hence highlighting that ripples are very different in frequency and have almost memory-less arrival times, but their duration has small variability.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4836732&req=5

pcbi.1004880.g001: CA1 ripples have standardized durations.From a 25hr experiment recording, ripples are identified as large amplitude excursion of the band-passed LFP. (a) The leftmost plots show wide band (1-400Hz) LFP recordings from CA1. The rightmost plots show the same LFPs band-pass filtered between 50Hz and 350Hz. (b) Histogram of ripple frequencies (count normalized to total number of ripples). The blue line is its Gaussian distribution fit. (c) Histogram of ripple inter-arrival times, and exponential fit in red. (d) Histogram of ripple durations, showing a high kurtosis, hence highlighting that ripples are very different in frequency and have almost memory-less arrival times, but their duration has small variability.
Mentions: We started investigating the nature of ripple oscillations by studying LFP recordings in hippocampal CA1 in rats. Representative examples of the wide-band and band-passed recordings are shown in Fig 1A. We focused on a few salient characteristics of ripple waves, such as frequency, duration and inter-arrival time (defined as the time between a ripple event and the next). Fig 1 shows that ripple frequency, defined as the inverse of the average inter-peak interval during a ripple event, was normally distributed around 163.5 (± 20.6) Hz (Fig 1B), their inter-arrival times were approximately exponential, with fitted rate 1.7748 Hz (Fig 1C), and their duration (Fig 1C) was centered about 51 (± 9.4) ms showing a high-kurtosis distribution (K = 20.1952, where for a normal distribution K = 3) [28]. Note that ripple frequency is representative of the peak-to-peak time within a given ripple (see S1 Fig for a representation), while the count of ripple events in a given time interval would be called ripple density, and can be found as the inverse of the inter-arrival times in such interval.

Bottom Line: Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep.We found that noise-induced loss of synchrony among CA1 interneurons dynamically constrains individual ripple duration.Our study proposes a novel mechanism of hippocampal ripple generation consistent with a broad range of experimental data, and highlights the role of noise in regulating the duration of input-driven oscillatory spiking in an inhibitory network.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology and Neuroscience, University of California Riverside, Riverside, California, United States of America.

ABSTRACT
Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep. Neurons active during behavior reactivate in both structures during sleep, in conjunction with characteristic brain oscillations that may form the neural substrate of memory consolidation. In the hippocampus, replay occurs within sharp wave-ripples: short bouts of high-frequency activity in area CA1 caused by excitatory activation from area CA3. In this work, we develop a computational model of ripple generation, motivated by in vivo rat data showing that ripples have a broad frequency distribution, exponential inter-arrival times and yet highly non-variable durations. Our study predicts that ripples are not persistent oscillations but result from a transient network behavior, induced by input from CA3, in which the high frequency synchronous firing of perisomatic interneurons does not depend on the time scale of synaptic inhibition. We found that noise-induced loss of synchrony among CA1 interneurons dynamically constrains individual ripple duration. Our study proposes a novel mechanism of hippocampal ripple generation consistent with a broad range of experimental data, and highlights the role of noise in regulating the duration of input-driven oscillatory spiking in an inhibitory network.

Show MeSH