Hippocampal Replay of Extended Experience

Davidson, Thomas J.; Kloosterman, Fabian; Wilson, Matthew A.

doi:10.1016/j.neuron.2009.07.027

Cited by 749 publications

(1,098 citation statements)

References 48 publications

Supporting

Mentioning

1,017

Contrasting

Unclassified

Order By: Relevance

“…The "replay" of waking activity has been assumed to play a critical role in memory consolidation and transfer of information from the hippocampus to the neocortex (12,13,(15)(16)(17)(18), because selective elimination of ripples after task learning impairs memory performance (22)(23)(24). Recent studies also emphasized the prospective and constructive role of ripple sequences (16)(17)(18)(19). Sequential activity of CA1 pyramidal neurons during ripples and in memory tasks during theta oscillations has been implicitly assumed to be generated in the recurrent excitatory networks of the hippocampal CA3 region and inherited through synaptic activity by the CA1 neuronal population (4,12,16,21,23) although direct evidence has not been shown experimentally.…”

Section: Discussionmentioning

confidence: 99%

“…Internally generated sequences have been also described in CA1 during theta oscillations in memory tasks (4, 11), raising the possibility that a given neuronal substrate is responsible for generating sequences at multiple time scales. The extensive recurrent excitatory collateral system of the CA3 region has been postulated to be critical in this process (4,7,12,13).The sequential activity of place cells is "replayed" during sharp waves (SPW) in a temporally compressed form compared with rate modulation of place cells (14)(15)(16)(17)(18)(19)(20) and may arise from the CA3 recurrent excitatory networks during immobility and slow wave sleep. The SPW-related convergent depolarization of CA1 neurons gives rise to a local, fast oscillatory event in the CA1 region ("ripple, refs.…”

mentioning

confidence: 99%

“…The sequential activity of place cells is "replayed" during sharp waves (SPW) in a temporally compressed form compared with rate modulation of place cells (14)(15)(16)(17)(18)(19)(20) and may arise from the CA3 recurrent excitatory networks during immobility and slow wave sleep. The SPW-related convergent depolarization of CA1 neurons gives rise to a local, fast oscillatory event in the CA1 region ("ripple," 140-180 Hz; refs.…”

mentioning

confidence: 99%

See 2 more Smart Citations

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Stark

Roux

Eichler

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

103

View full text Add to dashboard Cite

Sequential activity of multineuronal spiking can be observed during theta and high-frequency ripple oscillations in the hippocampal CA1 region and is linked to experience, but the mechanisms underlying such sequences are unknown. We compared multineuronal spiking during theta oscillations, spontaneous ripples, and focal optically induced high-frequency oscillations ("synthetic" ripples) in freely moving mice. Firing rates and rate modulations of individual neurons, and multineuronal sequences of pyramidal cell and interneuron spiking, were correlated during theta oscillations, spontaneous ripples, and synthetic ripples. Interneuron spiking was crucial for sequence consistency. These results suggest that participation of single neurons and their sequential order in population events are not strictly determined by extrinsic inputs but also influenced by local-circuit properties, including synapses between local neurons and single-neuron biophysics.A hypothesized hallmark of cognition is self-organized sequential activation of neuronal assemblies (1). Self-organized neuronal sequences have been observed in several cortical structures (2-5) and neuronal models (6-7). In the hippocampus, sequential activity of place cells (8) may be induced by external landmarks perceived by the animal during spatial navigation (9) and conveyed to CA1 by the upstream CA3 region or layer 3 of the entorhinal cortex (10). Internally generated sequences have been also described in CA1 during theta oscillations in memory tasks (4, 11), raising the possibility that a given neuronal substrate is responsible for generating sequences at multiple time scales. The extensive recurrent excitatory collateral system of the CA3 region has been postulated to be critical in this process (4,7,12,13).The sequential activity of place cells is "replayed" during sharp waves (SPW) in a temporally compressed form compared with rate modulation of place cells (14)(15)(16)(17)(18)(19)(20) and may arise from the CA3 recurrent excitatory networks during immobility and slow wave sleep. The SPW-related convergent depolarization of CA1 neurons gives rise to a local, fast oscillatory event in the CA1 region ("ripple, refs. 8 and 21). Selective elimination of ripples during or after learning impairs memory performance (22-24), suggesting that SPW ripple-related replay assists memory consolidation (12, 13). Although the local origin of the ripple oscillations is well demonstrated (25, 26), it has been tacitly assumed that the ripple-associated, sequentially ordered firing of CA1 neurons is synaptically driven by the upstream CA3 cell assemblies (12, 15), largely because excitatory recurrent collaterals in the CA1 region are sparse (27). However, sequential activity may also emerge by local mechanisms, patterned by the different biophysical properties of CA1 pyramidal cells and their interactions with local interneurons, which discharge at different times during a ripple (28-30). A putative function of the rich variety of interneurons is temporal organization of princip...

show abstract

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Stark

Roux

Eichler

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

103

View full text Add to dashboard Cite

show abstract

“…When at rest, or during pauses in exploration of a track, place cells in the rat hippocampus fire in sequences corresponding to portions of the route already traveled or about to be traveled (75). However, although these firing sequences take place over intervals that are linearly related to the distances represented, firing rates are very fast in comparison with the rat's normal rate of motion (corresponding to rates of about 8 m/s).…”

Section: Inability Tomentioning

confidence: 99%

Evolution of working memory

Carruthers

2013

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Working memory (WM) is fundamental to many aspects of human life, including learning, speech and text comprehension, prospection and future planning, and explicit "system 2" forms of reasoning, as well as overlapping heavily with fluid general intelligence. WM has been intensively studied for many decades, and there is a growing consensus about its nature, its components, and its signature limits. Remarkably, given its central importance in human life, there has been very little comparative investigation of WM abilities across species. Consequently, much remains unknown about the evolution of this important human capacity. Some questions can be tentatively answered from the existing comparative literature. Even studies that were not intended to do so can nonetheless shed light on the WM capacities of nonhuman animals. However, many questions remain.T he nature of human working memory (WM) has been extensively investigated, with thousands of articles and books on the topic produced over the last half-century. Some of the main findings of this research will be outlined shortly. However, we know hardly anything about how WM evolved. For that (if we are to go beyond plausible speculation), we need detailed comparative studies. However, remarkably few such studies have been conducted, as we will see. Nevertheless, the emerging consensus about the nature of human WM allows us to frame a series of questions or alternative hypotheses concerning the possible differences between human and animal WM. Some of these can be answered, at least tentatively, from the results of existing work. However, they should also be used to frame and guide future comparative experiments. Working Memory in HumansWM is the domain-general subsystem of the mind that enables one to activate and sustain (sometimes via active rehearsal) a set of mental representations for further manipulation and processing. The contents of working memory are generally thought to be conscious. Indeed, many identify the two constructs, maintaining that representations become conscious by gaining entry into WM (1). WM is generally thought to consist of an executive component that is distributed in areas of the frontal lobes working together with sensory cortical regions in any of the various sense modalities, which interact through attentional processes (2). It is also widely accepted that WM is quite limited in span, restricted to three or four chunks of information at any one time (3). Moreover, there are significant and stable individual differences in WM abilities between people, and these have been found to predict comparative performance in many other cognitive domains (4). Indeed, they account for most (if not all) of the variance in fluid general intelligence, or g (5).The primary mechanism of WM is thought to be executively controlled attention (2, 6). It is by targeting attention at representations in sensory areas that the latter gain entry into WM, and in the same manner they can be maintained there through sustained attention. Attention itself is though...

show abstract

“…Thus, despite its strong evidence for preplay, it does not conclusively answer the question of what role replay and preplay might subserve in real world navigation. One supportive indication came from Davidson, Kloosterman, and Wilson's (2009) demonstration that when rats are required to run on a straight track, ripple events get chained together for longer tracks. They suggested that this chaining might be mediated by reentrant processing between the hippocampus and entorhinal cortex, supporting the idea that replay during the SPW state might be a general mechanism employed in learning a navigational route.…”

Section: The Consumption Of Spatial Representationsmentioning

confidence: 99%

Investigating neural representations: the tale of place cells

Bechtel

2014

Synthese

View full text Add to dashboard Cite

While neuroscientists often characterize brain activity as representational, many philosophers have construed these accounts as just theorists' glosses on the mechanism. Moreover, philosophical discussions commonly focus on finished accounts of explanation, not research in progress. I adopt a different perspective, considering how characterizations of neural activity as representational contributes to the development of mechanistic accounts, guiding the questions neuroscientists ask as they work from an initial proposal to a more detailed understanding of a mechanism. I develop one illustrative example involving research on the information processing mechanisms mammals employ in navigating their environments. This research was galvanized by the discovery in the 1970s of place cells in the hippocampus. This discovery prompted research about how place representations are constructed in the relevant hippocampal neurons and how they figure in navigation. It also led to the discovery of a host of other types of neurons-grid cells, head--direction cells, boundary cells-that interact with place cells in the mechanism underlying spatial navigation. As I will try to make clear, the research is explicitly devoted to identifying representations and determining how they are constructed and used in an information processing mechanism. Construals of neural activity as representations are not mere glosses but are characterizations to which neuroscientists are committed in the development of their explanatory accounts.

show abstract

Hippocampal Replay of Extended Experience

Cited by 749 publications

References 48 publications

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Evolution of working memory

Investigating neural representations: the tale of place cells

Contact Info

Product

Resources

About