Brain-wide interactions during hippocampal sharp wave ripples

Nitzan, Noam; Swanson, Rachel A.; Schmitz, Dietmar; Buzsáki, György

doi:10.1073/pnas.2200931119

Cited by 58 publications

(45 citation statements)

References 65 publications

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“…When hippocampal ripples occurred, there was an increased probability of ripples in extrahippocampal MTL regions; a shift in LFP power from lower to higher frequencies in these regions; and an increase in MTL-wide neuronal spiking activity. Related long-range effects of hippocampal ripples have been described in both animals and humans ( 21, 22, 24, 37, 53, 55 ). Through these excitatory effects, hippocampal ripples may play a key role in the formation and retrieval of associative memories by coordinating and combining diverse patterns of neural activity from multiple regions.…”

Section: Resultsmentioning

confidence: 99%

“…Our finding of wide-ranging neural changes during hippocampal ripples aligns with previous reports in both animals and humans. In rodents, hippocampal sharp-wave ripples are accompanied by widespread cortical and subcortical activations (22,88,89) and coincide with transient brain-wide increases in functional connectivity (24). In humans, hippocampal ripples are coupled with ripples in many cortical areas (23,33,37) and are accompanied by increased high-frequency broadband activity in widely distributed neocortical sites (40).…”

Section: Neural Changes During Hippocampal Ripplesmentioning

confidence: 99%

“…We reasoned that hippocampal ripples might coordinate the coactivity of object and place cells because they synchronize neural activity across close and distant brain regions (13,14,(21)(22)(23)(24). Hippocampal ripples may thus help induce and activate large-scale cellular networks (16), which we considered instrumental in linking and coordinating otherwise unconnected neurons for the encoding and retrieval of associative memories.…”

Section: Introductionmentioning

confidence: 99%

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Ripple-locked coactivity of stimulus-specific neurons supports human associative memory

Kunz

Staresina

Reinacher

et al. 2022

Preprint

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Associative memory is the ability to encode and retrieve relations between different stimuli. To better understand its neural basis, we investigated whether associative memory involves precisely timed spiking of neurons in the medial temporal lobes that exhibit stimulus-specific tuning. Using single-neuron recordings from epilepsy patients performing an associative object–location memory task, we identified the object- and place-specific neurons that encoded the separate elements of each memory. When patients encoded and retrieved particular memories, the relevant object- and place-specific neurons activated synchronously during hippocampal ripples. This ripple-locked coactivity of stimulus-specific neurons emerged over time as the patients’ associative learning progressed. Our results suggest a cellular account of associative memory, in which hippocampal ripples coordinate the activity of specialized cellular populations to facilitate links between stimuli.

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Section: Resultsmentioning

confidence: 99%

Section: Neural Changes During Hippocampal Ripplesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Ripple-locked coactivity of stimulus-specific neurons supports human associative memory

Kunz

Staresina

Reinacher

et al. 2022

Preprint

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“…Increasing evidence suggested that the hippocampal ripples are coordinated with brain-wide neural dynamics (25,(30)(31)(32). The present study extended these findings by showing that the hippocampal replays are embedded in the global cascade dynamics of sequential activation.…”

Section: Discussionmentioning

confidence: 99%

Self-generated brain-wide spiking cascades govern replay dynamics in the hippocampus

Yang

Leopold

Duyn

et al. 2022

Preprint

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During states of behavioral quiescence, neurons in the hippocampus replay sequences of spiking activity experienced in earlier behavioral episodes. While such replay sequences are hypothesized to serve learning and memory by facilitating synaptic consolidation, their generative mechanisms remain poorly understood. Increasing evidence suggests that they might be generated internally, or at least strongly constrained by internal circuit dynamics. Recent work demonstrated that, across the forebrain, approximately 70% of neurons participate in a pattern of sequential spiking cascades during rest. Like hippocampal replay sequences, these brain-wide spiking cascades occur together with high-frequency hippocampal ripples and therefore may share a common generative mechanism. Here we systematically investigated the relationship between replay activity and sequential spiking cascades by analyzing a database of intracortical electrocortical recordings in mice. For neuronal subpopulations in the hippocampus and visual cortex, we assessed spiking sequences elicited during video viewing as well as potential replay events during subsequent periods of rest. We found that replay events were unique to hippocampal time-sensitive neurons and occurred together with spiking cascades throughout the forebrain. Furthermore, forward and time-reversed replay sequences were associated with different types of spiking cascades. Overall, these findings indicate that hippocampal replay events are generated and structured according to resting state circuit dynamics manifest across a large portion of the brain.

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“…A natural extension for the analyses presented here would be the question of whether such cross-strata co-occurrence manifests in the CA3 and the CA2, which play critical roles in the emergence of ripples (Ylinen et al, 1995;Chrobak and Buzsaki, 1996;Buzsaki, 2015) apart from manifesting theta oscillations (Buzsaki, 2002;Goutagny et al, 2009;Colgin, 2013). Furthermore, although our recordings and analyses were limited to the dorsal hippocampus, it is critical to assess co-occurrences with simultaneous multi-strata recordings along the dorsoventral and proximo-distal axes of the hippocampus involving brain-wide interactions during such events (Nitzan et al, 2022). Importantly, future studies analyses should assess the intracellular counterparts of theta vs. non-theta ripples in the somatic and the dendritic compartments of identified deep vs. superficial neurons.…”

Section: Experimental Designs and Analysis Pipelines Should Explicitl...mentioning

confidence: 99%

Cross-strataco-occurrence of ripples with theta-frequency oscillations in the hippocampus of foraging rats

Seenivasan

Basak

Narayanan

2022

Preprint

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Background and motivation: Brain rhythms have been postulated to play central roles in animal cognition. A prominently reported dichotomy of hippocampal rhythms, driven primarily by historic single-stratarecordings, assigns theta-frequency oscillations (4–12 Hz) and ripples (120–250 Hz) to be exclusively associated with preparatory and consummatory behaviors, respectively. However, due to the differential power expression of these two signals across hippocampalstrata, reports of such exclusivity require validation through simultaneous multi-stratarecordings and cross-strataanalysis of these oscillatory patterns.Methodology: We assessed co-occurrence of theta-frequency oscillations with ripples in multi-channel recordings of extracellular potentials across hippocampalstratafrom foraging rats. We detected all ripple events from an identifiedstratum pyramidale(SP) channel based on rigorous thresholds relating to the spectro-temporal and spatial characteristics of ripples. We then defined theta epochs based on theta oscillations detected from each of the different channels spanning the SP to thestratum lacunosum-moleculare(SLM) through thestratum radiatum(SR). We calculated the proportion of ripples embedded within theta epochs.Results: We found ~20% (across rats) of ripple events (in SP) to co-occur with theta epochs identified from SR/SLM channels, defined here astheta ripples. All characteristics of theta ripples were comparable with ripples that occurred in the absence of theta oscillations. Furthermore, the power of theta oscillations in the immediate vicinity of theta ripples was similar to theta power across identified theta epochs, together validating the identification process of theta ripples. Strikingly, when theta epochs were instead identified from the SP channel, such co-occurrences were significantly lower in number. The reduction in the number of theta ripples was consequent to progressive reduction in theta power along the SLM-SR-SP axis. We assessed the behavioral state of rats during ripple events and found most theta ripples to occur during immobile periods. We confirmed that across sessions and rats, the theta power observed during exploratory theta epochs was comparable with theta power during immobile theta epochs. In addition, the progressive reduction in theta power along the SLM-SR-SP axis was common to both exploratory and immobile periods. Finally, we found a strong theta-phase preference of theta ripples within the third quadrant [3π/2–2π] of the associated theta oscillation.Implications: Our analyses provide direct quantitative evidence for the occurrence of ripple events nested within theta oscillations in the rodent hippocampus. These analyses emphasize that the prevalent dichotomy about the manifestation of theta-frequency oscillations and ripples needs to be reevaluated, after explicitly accounting for the differentialstratum-dependent expression of these two oscillatory patterns. The prevalence of theta ripples expands the potential roles of ripple-frequency oscillations to span the continuum of encoding, retrieval, and consolidation, achieved through interactions with theta oscillations.

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Brain-wide interactions during hippocampal sharp wave ripples

Cited by 58 publications

References 65 publications

Ripple-locked coactivity of stimulus-specific neurons supports human associative memory

Ripple-locked coactivity of stimulus-specific neurons supports human associative memory

Self-generated brain-wide spiking cascades govern replay dynamics in the hippocampus

Cross-strataco-occurrence of ripples with theta-frequency oscillations in the hippocampus of foraging rats

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