A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP

doi:10.1016/J.TINS.2011.07.006

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A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP

Journal Article•DOI•

A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP

John E. Lisman¹, Anthony A. Grace², Emrah Düzel³, Emrah Düzel⁴•Institutions (4)

Brandeis University¹, University of Pittsburgh², University College London³, Otto-von-Guericke University Magdeburg⁴

01 Oct 2011-Trends in Neurosciences (NIH Public Access)-Vol. 34, Iss: 10, pp 536-547

TL;DR: Recent experimental findings are discussed that support the view that this 'neoHebbian' framework can account for memory behavior in a variety of learning situations.

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About: This article is published in Trends in Neurosciences.The article was published on 2011-10-01 and is currently open access. It has received 377 citations till now. The article focuses on the topics: Hebbian theory & Long-term potentiation.

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Journal Article•DOI•

How schema and novelty augment memory formation.

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Marlieke T. R. van Kesteren¹, Marlieke T. R. van Kesteren², Dirk J. Ruiter², Guillén Fernández², Guillén Fernández¹, Richard N. Henson³ - Show less +2 more•Institutions (3)

Radboud University Nijmegen¹, Radboud University Nijmegen Medical Centre², Cognition and Brain Sciences Unit³

01 Apr 2012-Trends in Neurosciences

TL;DR: Lesion and neuroimaging findings in animals and humans that relate to the apparent paradoxical relationship between schema and novelty and a framework relating key brain regions in medial temporal lobe and medial prefrontal cortex during encoding, consolidation and retrieval of information as a function of its congruency with existing information represented in neocortex are reviewed.

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652 citations

Journal Article•DOI•

The synaptic plasticity and memory hypothesis: encoding, storage and persistence.

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Tomonori Takeuchi¹, Adrian J. Duszkiewicz¹, Richard G. M. Morris¹•Institutions (1)

University of Edinburgh¹

05 Jan 2014-Philosophical Transactions of the Royal Society B

TL;DR: Evidence derived using optical imaging, molecular-genetic and optogenetic techniques in conjunction with appropriate behavioural analyses continues to offer support for the idea that changing the strength of connections between neurons is one of the major mechanisms by which engrams are stored in the brain.

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Abstract: The synaptic plasticity and memory hypothesis asserts that activity-dependent synaptic plasticity is induced at appropriate synapses during memory formation and is both necessary and sufficient for the encoding and trace storage of the type of memory mediated by the brain area in which it is observed. Criteria for establishing the necessity and sufficiency of such plasticity in mediating trace storage have been identified and are here reviewed in relation to new work using some of the diverse techniques of contemporary neuroscience. Evidence derived using optical imaging, molecular-genetic and optogenetic techniques in conjunction with appropriate behavioural analyses continues to offer support for the idea that changing the strength of connections between neurons is one of the major mechanisms by which engrams are stored in the brain.

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517 citations

Journal Article•DOI•

What Learning Systems do Intelligent Agents Need? Complementary Learning Systems Theory Updated

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Dharshan Kumaran¹, Dharshan Kumaran², Demis Hassabis¹, James L. McClelland³•Institutions (3)

Google¹, University College London², Stanford University³

01 Jul 2016-Trends in Cognitive Sciences

TL;DR: This work updates complementary learning systems (CLS) theory and extends it by showing that recurrent activation of hippocampal traces can support some forms of generalization and that neocortical learning can be rapid for information that is consistent with known structure.

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500 citations

Cites background from "A neoHebbian framework for episodic..."

...A wide range of factors may affect the significance of individual experiences [82,83]: for example, they may be surprising or novel; high in reward value (either positive or negative) or in their informational content (e....
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...The hippocampus – in receipt of highly processed multimodal sensory information [84] as well as neuromodulatory signals triggered by such factors [83,85] – is well positioned to reweight individual experiences accordingly....
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...Indeed, recent work suggests specific molecular mechanisms that support the stabilization of memories and specific neuromodulatory projections to the hippocampus [83,86–88] that allow the persistence of individual experiences in the hippocampus to be modulated by events that occur both before and afterwards, providing mechanisms by which episodes may be retrospectively reweighted if their significance is enhanced by subsequent events [83,89], thereby influencing the probability of replay....
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Journal Article•DOI•

States of Curiosity Modulate Hippocampus-Dependent Learning via the Dopaminergic Circuit

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Matthias J. Gruber¹, Bernard D. Gelman¹, Charan Ranganath¹•Institutions (1)

University of California, Davis¹

22 Oct 2014-Neuron

TL;DR: Findings suggest a link between the mechanisms supporting extrinsic reward motivation and intrinsic curiosity and highlight the importance of stimulating curiosity to create more effective learning experiences.

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420 citations

Cites background or result from "A neoHebbian framework for episodic..."

...…to memory formation during curious states strongly parallel theoretical accounts and findings in rodents showing that dopaminergic activity can modulate hippocampus-dependent learning (for reviews, see Düzel et al., 2010; Lisman and Grace, 2005; Lisman et al., 2011; Shohamy and Adcock, 2010)....
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...If so, then dopaminergic activity during states of high curiosity might have “rescued” memories for incidentally encoded faces that would otherwise been forgotten (Lisman et al., 2011; Redondo and Morris, 2011)....
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...Accordingly, several models (Frey and Morris, 1998; Lisman and Grace, 2005; Lisman et al., 2011; Redondo and Morris, 2011; Shohamy and Adcock, 2010) propose that stabilization of learning-induced hippocampal plasticity depends on dopaminergic neuromodulation, in addition to synaptic activity....
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...2013) and have been hypothesized to comprise a functional loop in the service of learning (Düzel et al., 2010; Lisman and Grace, 2005; Lisman et al., 2011)....
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...The present findings have potential implications for understanding memory deficits in the elderly and in patients with psychiatric and neurological disorders that affect dopaminergic transmission (Chowdhury et al., 2013; Düzel et al., 2010; Goto and Grace, 2008; Lisman et al., 2011)....
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Journal Article•DOI•

High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research

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Jean-Philippe Lachaux¹, Nikolai Axmacher², Nikolai Axmacher³, Florian Mormann³, Eric Halgren⁴, Nathan E. Crone⁵ - Show less +2 more•Institutions (5)

French Institute of Health and Medical Research¹, University of Bonn², German Center for Neurodegenerative Diseases³, University of California, San Diego⁴, Johns Hopkins University School of Medicine⁵

26 Jun 2012-Progress in Neurobiology

TL;DR: Overall, iEEG research on HFA should play an increasing role in cognitive neuroscience in humans, because it can be explicitly linked to basic research in animals, and the future evolution of this field is discussed.

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393 citations

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References

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Book•

The Organization of Behavior: A Neuropsychological Theory

[...]

D. O. Hebb¹•Institutions (1)

McGill University¹

01 Jan 1949

TL;DR: In this paper, the authors discuss the first stage of perception: growth of the assembly, the phase sequence, and the problem of Motivational Drift, which is the line of attack.

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Abstract: Contents: Introduction. The Problem and the Line of Attack. Summation and Learning in Perception. Field Theory and Equipotentiality. The First Stage of Perception: Growth of the Assembly. Perception of a Complex: The Phase Sequence. Development of the Learning Capacity. Higher and Lower Processes Related to Learning. Problems of Motivation: Pain and Hunger. The Problem of Motivational Drift. Emotional Disturbances. The Growth and Decline of Intelligence.

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5,038 citations

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Evidence for the existence of monoamine-containing neurons in the central nervous system. i. demonstration of monoamines in the cell bodies of brain stem neurons.

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Dahlstroem A, Fuxe K

01 Jan 1964-Acta Physiologica Scandinavica

4,814 citations

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Memory and consciousness

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Endel Tulving¹•Institutions (1)

University of Toronto¹

01 Jan 1985-Canadian Psychology

3,876 citations

Journal Article•DOI•

An Integrative Theory of Locus Coeruleus-Norepinephrine Function: Adaptive Gain and Optimal Performance.

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Gary Aston-Jones¹, Jonathan D. Cohen•Institutions (1)

University of Pennsylvania¹

15 Jul 2005-Annual Review of Neuroscience

TL;DR: In this article, the locus coeruleus-norepinephrine (LC-NE) system plays a more complex and specific role in the control of behavior than investigators previously thought.

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Abstract: Historically, the locus coeruleus-norepinephrine (LC-NE) system has been implicated in arousal, but recent findings suggest that this system plays a more complex and specific role in the control of behavior than investigators previously thought. We review neurophysiological and modeling studies in monkey that support a new theory of LC-NE function. LC neurons exhibit two modes of activity, phasic and tonic. Phasic LC activation is driven by the outcome of task-related decision processes and is proposed to facilitate ensuing behaviors and to help optimize task performance (exploitation). When utility in the task wanes, LC neurons exhibit a tonic activity mode, associated with disengagement from the current task and a search for alternative behaviors (exploration). Monkey LC receives prominent, direct inputs from the anterior cingulate (ACC) and orbitofrontal cortices (OFC), both of which are thought to monitor task-related utility. We propose that these frontal areas produce the above patterns of LC activity to optimize utility on both short and long timescales.

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3,441 citations

Journal Article•DOI•

Depth of processing and the retention of words in episodic memory.

[...]

Fergus I. M. Craik¹, Endel Tulving•Institutions (1)

University of Toronto¹

01 Jan 1975-Journal of Experimental Psychology: General

TL;DR: For instance, Craik and Lockhart as discussed by the authors explored the levels of processing framework for human memory research and found that deeper encodings took longer to accomplish and were associated with higher levels of performance on the subsequent memory test.

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Abstract: SUMMARY Ten experiments were designed to explore the levels of processing framework for human memory research proposed by Craik and Lockhart (1972). The basic notions are that the episodic memory trace may be thought of as a rather automatic by-product of operations carried out by the cognitive system and that the durability of the trace is a positive function of "depth" of processing, where depth refers to greater degrees of semantic involvement. Subjects were induced to process words to different depths by answering various questions about the words. For example, shallow encodings were achieved by asking questions about typescript; intermediate levels of encoding were accomplished by asking questions about rhymes; deep levels were induced by asking whether the word would fit into a given category or sentence frame. After the encoding phase was completed, subjects were unexpectedly given a recall or recognition test for the words. In general, deeper encodings took longer to accomplish and were associated with higher levels of performance on the subsequent memory test. Also, questions leading to positive responses were associated with higher retention levels than questions leading to negative responses, at least at deeper levels of encoding. Further experiments examined this pattern of effects in greater analytic detail. It was established that the original results did not simply reflect differential encoding times; an experiment was designed in which a complex but shallow task took longer to carry out but yielded lower levels of recognition than an easy, deeper task. Other studies explored reasons for the superior retention of words associated with positive responses on the initial task. Negative responses were remembered as well as positive responses when the questions led to an equally elaborate encoding in the two cases. The idea that elaboration or "spread" of encoding provides a better description of the results was given a further boost by the finding of the typical pattern of results under intentional learning conditions, and where each word was exposed for 6 sec in the initial phase. While spread and elaboration may indeed be better descriptive terms for the present findings, retention depends critically on the qualitative nature of the encoding operations performed; a minimal semantic analysis is more beneficial than an extensive structural analysis. Finally, Schulman's (1974) principle of congruity appears necessary for a complete description of the effects obtained. Memory performance is enhanced to the extent that the context, or encoding question, forms an integrated unit with the word presented. A congruous encoding yields superior memory performance because a more elaborate trace is laid down and because in such cases the structure of semantic memory can be utilized more effectively to facilitate retrieval. The article concludes with a discussion of the broader implications of these data and ideas for the study of human learning and memory,

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3,259 citations