Hippocampal synaptic enhancement and information storage within a distributed memory system

McNaughton, Bruce L.; Morris, Richard

doi:10.1016/0166-2236(87)90011-7

Cited by 1,153 publications

(991 citation statements)

References 55 publications

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“…Although not studied explicitly here, unpublished observations on CA1 cells indicate that this effect occurs generally in the LIA state, during sharp-waves, and is not exclusive to SWS. Because of the extensive excitatory recurrent connections between pyramidal cells in CA3, this region has been regarded as a hippocampal subfield essential for formation and/or retrieval of associative memory (Marr 1971;McNaughton and Morris 1987;McNaughton and Nadel 1990;Rolls 1996;Rolls 1989;Rolls 1991, 1994), which is then forwarded to CA1 region. The present results neither confirm nor disprove this conjecture, but do provide further support for the conclusion that coherent reactivation of recent experience occurs widely, probably at least throughout the entire archicortex and neocortex.…”

Section: Discussionmentioning

confidence: 99%

Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience

Shen

Kudrimoti

McNaughton

et al. 1998

Journal of Sleep Research

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SUMMARYPatterns of neuronal activity recorded in CA1 of the hippocampus and in neocortex during waking-behavior, are reactivated during subsequent slow-wave sleep (SWS). It has been suggested that this reactivation may originate in the hippocampal CA3 region, where modifiable excitatory recurrent connections are abundant and where sharpwaves, in which the reactivation is most robust, appear to arise. The present experiment investigated whether ensemble firing patterns of granule cells in the fascia dentata (FD), an area`upstream' from CA3, are also reactivated during sleep. Populations of FD granule cells were recorded from during spatial behavior and during prior and subsequent SWS. Firing rate correlations between cell-pairs with overlapping place fields were significantly enhanced during post behavioral sleep compared to pre behavioral sleep. Correlations between cells with non-overlapping place fields or which were silent during maze behavior, were not changed. Thus, reactivation of experiencespecific correlation states also occurs in granule cells during sleep. Because these cells do not have excitatory interconnections, but form a major input to CA3 pyramidal cells, current models predicted that sleep reactivation would appear first in CA3. There are, however, both extensive polysynaptic excitatory interactions among granule cells and feedback from CA3 pyramidal cells. Granule cells also receive indirect input from neocortical regions known to undergo trace reactivation. Although a simple model for a CA3 origin of the reactivation phenomenon cannot be confirmed, the present results extend our understanding of the generality of this phenomenon.

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Section: Discussionmentioning

confidence: 99%

Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience

Shen

Kudrimoti

McNaughton

et al. 1998

Journal of Sleep Research

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“…Distinctions can be drawn between acti6e memory (in which a representation of the stimulus is held in neural activity) [55,64,252], filtering mechanisms (in which individual neurons respond differently to novel and to familiar objects [114,115], probably an implementation of perceptual priming [240]), and content-addressable memories (memory stored in interneuronal connections, presumably through LTPlike mechanisms) [75,83,110,156,171,184]. Each of these processes have advantages and disadvantages.…”

Section: Multiple Memory Systemsmentioning

confidence: 99%

The hippocampal debate: are we asking the right questions?

Redish

2001

Behavioural Brain Research

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For years, the debate has been: 'Is the hippocampus the cognitive map?' or 'Is the hippocampus the core of memory?' These two hypotheses derived their original power from two key experiments-the cognitive map theory from the remarkable spatial correlates seen in recordings of hippocampal pyramidal cells and the memory theory from the profound amnesias seen in the patient H.M. Both of these key experiments have been reinterpreted over the years: hippocampal cells are correlated with much more than place and H.M. is missing much more than just his hippocampus. However, both theories are still debated today. The hippocampus clearly plays a role in both navigation and memory processing. The question that must be addressed is rather: 'What is the role played by the hippocampus in the navigation and memory systems?' By looking at the navigation system as a whole, one can identify the major role played by the hippocampus as correcting for accumulation errors that occur within idiothetic navigation systems. This is most clearly experimentally evident as reorientation when an animal is lost. Carrying this over to a more general process, this becomes a role of recalling a context, bridging a contextual gap, or, in other words, it becomes a form of recognition memory. I will review recent experimental data which seems to support this theory over the more general spatial or memory theories traditionally applied to hippocampus.

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“…In piecing together this jigsaw of hippocampal subfields and connections, the collective tendency has been to start with the DG and build around a trisynaptic circuit to CA3 and then subsets of granule cells and may be 'orthoganolized' at this stage) followed by pattern completion in CA3 (where dense recurrent, excitatory projections within its own pyramidal cell population endow 'auto-associative' properties) [1][2][3][4][5](see also [Ref] in this issue). The neat hippocampal loop has therefore been presumed to allow integration and processing of information provided via association cortex, then subsequent feedback to the cortex via CA1.…”

Section: Introductionmentioning

confidence: 99%

Updating hippocampal representations: CA2 joins the circuit

Jones

McHugh

2011

Trends in Neurosciences

111

106

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The hippocampus integrates the encoding, storage and recall of memories, binding the spatiotemporal and sensory information that constitutes experience and keeping episodes in their correct context. The rapid and accurate processing of such daunting volumes of continuouslychanging data relies on dynamically assigning different aspects of mnemonic processing to specialized, interconnected networks corresponding to the anatomical subfields of dentate gyrus (DG), CA3 and CA1. However, differentially processed information ultimately has to be reintegrated into conjunctive representations, and this is unlikely to be achieved by unidirectional, sequential steps through a DG-CA3-CA1 loop. In this Review, we highlight recently discovered anatomical and physiological features that are likely to necessitate updates to the hippocampal circuit diagram, particularly by incorporating the oft-neglected CA2 region.3

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Hippocampal synaptic enhancement and information storage within a distributed memory system

Cited by 1,153 publications

References 55 publications

Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience

Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience

The hippocampal debate: are we asking the right questions?

Updating hippocampal representations: CA2 joins the circuit

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