Coupled ripple oscillations between the medial temporal lobe and neocortex retrieve human memory

Vaz, Alex P.; Inati, Sara K.; Brunel, Nicolas; Zaghloul, Kareem A.

doi:10.1126/science.aau8956

Cited by 219 publications

(406 citation statements)

References 35 publications

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“…Next, we explored the neural substrate of social memory consolidation in the social recognition task. We observed a significant increase in the rate of SWRs during sleep after the social experience (post-sleep) compared to sleep before the social experience (pre-sleep; Fig.2a), similar to the increase in SWRs in rodents during sleep following spatial exploration 14 and in humans engaged in a visual memory task 15,16,17 . We thus hypothesized that SWRs are involved in social memory consolidation.…”

supporting

confidence: 72%

Hippocampal CA2 ripples recruit social replay and promote social memory

Oliva

Fernández‐Ruiz

Leroy

et al. 2020

Preprint

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The consolidation of spatial memory depends on the reactivation ('replay') of hippocampal place cells that were active during recent behavior. These reactivations are observed during sharp wave-ripples (SWRs), synchronous oscillatory events that occur during slow-wave sleep 1-9 and whose disruption impairs spatial memory consolidation 4,6,7,9 .Although the hippocampus encodes a wide range of non-spatial forms of declarative memory, it is not yet known whether SWRs are necessary for non-spatial memory.Moreover, although SWRs can arise from either the hippocampal CA3 8 or CA2 10 regions, the relative importance of these sources for memory consolidation is unknown. Here we examined the role of SWRs during the consolidation of social memory, the ability of an animal to recognize and remember a conspecific, focusing on CA2 because of its critical role in social memory 11,12,13 . We found that ensembles of CA2 pyramidal neurons that were active during social exploration of novel conspecifics were reactivated during SWRs. Importantly, disruption or enhancement of CA2 SWRs suppressed or prolonged social memory, respectively. Thus, SWR reactivation of hippocampal firing related to recent experience appears to be a general mechanism for binding spatial, temporal and sensory information into high-order memory representations.We employed a social recognition task that assessed social memory formation in mice without interference from other social behaviors. In this task, a subject mouse was first habituated to a square arena with two empty wire cup cages in opposite corners. Immediately after habituation, we placed a novel stimulus mouse in each of the empty cups (mouse S 1 and S 2 ). In social learning trial 1 the subject mouse was allowed to explore the arena for 5 min. This was immediately followed by a second 5 min social learning trial with the positions of the same Figure 1: Encoding of conspecifics by CA2 pyramidal cells activity. a) Schema of the task. b) Task performance in wild-type mice (n = 13). Social memory quantified during recall trial by a discrimination index (see Methods).

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supporting

confidence: 72%

Hippocampal CA2 ripples recruit social replay and promote social memory

Oliva

Fernández‐Ruiz

Leroy

et al. 2020

Preprint

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“…Through robust autapses, pvBCs adjust their temporal firing interval and correspondingly set inhibition in their target neurons. This mechanism may be essential in setting cell assembly discharges in the neocortex (Molnar G et al 2008;Toth K et al 2018; de la Prida LM and G Huberfeld 2019) during associative memory processing (Kucewicz MT et al 2014) and memory retrieval (Vaz AP et al 2019). In addition, pvBC self-inhibition may contribute to pyramidal cell disinhibition during the induction of L2/3 LTP associated with learning (Williams LE and A Holtmaat 2019).…”

Section: Resultsmentioning

confidence: 99%

Robust perisomatic GABAergic self-innervation inhibits basket cells in the human and mouse supragranular neocortex

Szegedi

Paizs

Baka

et al. 2019

Preprint

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Inhibitory autapses are self-innervating synaptic connections in GABAergic interneurons in the brain. Autapses in neocortical layers have not been systematically investigated, and their function in different mammalian species and specific interneuron types is poorly known. We investigated GABAergic parvalbumin-expressing basket cells (pvBCs) in layer 2/3 (L2/3) in mice as well as in human neocortical tissue resected in deep-brain surgery. Most pvBCs showed robust GABAAR-mediated self-innervation in both species, but autapses were rare in nonfast spiking GABAergic interneurons. Light-and electron microscopy analyses revealed pvBC axons innervating their own soma and proximal dendrites. GABAergic selfinhibition conductance was similar in human and mouse pvBCs and comparable to that of synapses from pvBCs to other L2/3 neurons. Autaptic conductance prolonged somatic inhibition in pvBCs after a spike and inhibited repetitive firing. Perisomatic autaptic inhibition has evolved in pvBCs of various cortical layers and different mammalian species to control discharge of these interneurons.

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“…Recent work has also identified unique theta-nested gamma oscillations observed within individual theta cycles (Lopes-Dos-Santos et al, 2018), providing support for the notion that fast and slow gamma separately mediate encoding of novel information and memory retrieval. Intracranial recordings in humans have identified ripple oscillations (~80 to 100 Hz) that are involved in memory retrieval and consolidation (Axmacher et al, 2008;Staresina et al, 2015;Vaz et al, 2019) and exhibit phase amplitude coupling (PAC) with hippocampal theta phase (Staresina et al, 2015). Similar ripple oscillations are also prevalent in nonhuman primates during visual search (Leonard and Hoffman, 2017;Leonard et al, 2015), raising the possibility that they play an active role in exploration.…”

Section: Introductionmentioning

confidence: 99%

Hippocampal theta coordinates memory processing during visual exploration

Kragel¹,

VanHaerents²,

Templer³

et al. 2019

Preprint

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The hippocampus supports memory encoding and retrieval, with distinct phases of theta oscillations modulating the amplitude of gamma-band activity during each process. Encoding and retrieval operations dynamically interact over rapid timescales, especially when sensory information conflicts with memory. The ability to link hippocampal dynamics to specific memory-guided behaviors has been limited by experiments that lack the temporal resolution to segregate when encoding and retrieval occur. To resolve this issue, we simultaneously tracked eye movements and hippocampal field potentials while neurosurgical patients performed a spatial memory task. Novelty-driven fixations increased phase-locking to the theta rhythm, which predicted successful memory performance. Theta to gamma phase amplitude coupling increased during these viewing behaviors and predicted forgetting of conflicting memories. In contrast, theta phase-locking preceded fixations initiated by memory retrieval, indicating that the hippocampus coordinates memory-guided eye movements. These findings suggest that theta oscillations in the hippocampus support learning through two interleaved processes: strengthening the encoding of novel information and guiding exploration based on prior experience.

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Coupled ripple oscillations between the medial temporal lobe and neocortex retrieve human memory

Cited by 219 publications

References 35 publications

Hippocampal CA2 ripples recruit social replay and promote social memory

Hippocampal CA2 ripples recruit social replay and promote social memory

Robust perisomatic GABAergic self-innervation inhibits basket cells in the human and mouse supragranular neocortex

Hippocampal theta coordinates memory processing during visual exploration

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