Testing

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Sleep Mediation of Episodic Memory and Associative Learning II:

A Potential Computational Synthesis

Itamar Lerner & Mark A. Gluck

1 Center for Molecular & Behavioral Neuroscience, Rutgers University, Newark, NJ, USA

Background - I

Sleep improves performance: Representative findings

General design: training

wake/sleep

testing

I. Episodic memory: Paired associates learning

Dog - Pianist

Hole - Sky

Hole - ?

Backhaus et al., 2011

Paired-associates task-design.

Observation of pairs to be memorized is followed by

12hours of wake or sleep, after which cued recall is tested.

Plihal &

Born, 1997

Recall performance increases due to SWS between training and testing

II. Gist extraction: Learning meaning of Chinese characters:

Lau et al., 2011

A shared pattern in Chinese characters is recognized better after sleep

III. Rule extrapolation: Learning Implicit hierarchy between stimuli

Training:

Memorizing relations between the item pairs a,b,c,d,e: a>b, b>c, c>d, d>e, e>f

(pairs contain implicit hierarchy: a>b>c>d>e>f) Ellenbogen et al., 2006

Testing:

Hierarchies with 1 ° separation: b>d, d>e

Hierarchies with 2 ° separation: b>e

Hierarchy rule is more easily recognized after sleep compared to wake

Introduction

Evidence from the last decade shows that sleep has an important role in learning and memory. specifically, sleep – and especially Slow-Wave Sleep (SWS) and, sometimes, Rapid-Eye-Movement sleep (REM) – has been shown to improve

episodic memory, gist extraction

, and

rule extrapolation and insight.

In addition, it has been shown that following sleep (especially SWS) synaptic strength within cortical and hippocampal circuits is generally decreased, these two findings have often been taken to support different and even contradicting theories about the role of sleep in learning and memory. The current work in progress is a computational approach that seeks to combine a broad range of empirical findings within a uniform neuro-computational framework.

Background - II

Synaptic strength is reduced during sleep: Representative findings

Slope and Amplitude of Excitatory Post-Synaptic Potentials

(EPSPs) in the prefrontal cortex of rats decrease following sleep compared to a Sleep-deprivation period. (W – Wake; S – Sleep;

Vyazovskiy et al., 2008)

Changes in cortical Local Field Potential (LFP) in rats in response to stimulation after a period of wake (Sleep

Deprived - SD) compared to sleep (Liu et al., 2010)

Qualitative Traits of the Model

Parsimonious representations facilitate cognitive performance

After sleep-dependent unification and differentiation, each objective is more readily accessed:

Before sleep: After sleep:

Pairedassociates:

Learned patterns

Test sample

Learned patterns

Test sample

Objective:

Complete the test sample with activation based on the correct learned pattern

Gist extraction:

Rule learning:

Which of the two test samples fit better to the learned patterns?

Learned patterns

Test samples

Learned patterns

Test samples

Learned structures

Test sample

Learned structures

Test sample

To which of the two learned structures does the test sample fit?

Model Principles

1. Based on our previous NSF-supported modeling (Gluck and Myers, 1993; Moustafa et al., 2009) we assert that storing episodic memories, extracting gist information, or extrapolating a classification rule, all crucially depend on gradual learning of stimulusstimulus associations in the

Medial Temporal Cortex

hippocampus during wake. Only after learning these statistical regularities, can the system (Medial Temporal

Cortex and Striatum) process appropriate responses.

Hippocampus

2. Sleep (especially SWS) provides an additional processing stage to the hippocampal representations that were acquired during wake, allowing them to become more parsimonious and consequently boost performance in the subsequent testing phase. This additional stage is based on two processes:

Differentiation

: Representations with a small degree of correlations become largely uncorrelated

Unification

: Representations that are very correlated to each other are unified to become a single representation.

A. Differentiation

3. Both of these changes are carried out by

deletion of synapses

: Differentiation is achieved by deletion of synapses that support activation of neurons common to several representations (thus causing these representations to become uncorrelated). Unification is achieved by deletion of synapses that support activation of neurons that are unique to each representation (thus allowing only neurons common to all these representations to survive, turning these separate representations into a single representation).

B. Unification

Differentiation and Unification processes. Each row represents a different memory pattern learned by the hippocampus during wake. Each circle represents a unit (neuron). Red circles active units; White units – inactive.

Gradual learning during wake

Sleep

Sleep extends pattern differentiation

Input correlation

Sleep sharpens hippocampal inputto-output correlational differences

Synaptic deletion during sleep may play a computational role in improving cognitive performance by differentiating and unifying representations

Acknowledgements

Supported by Grant #7367437 for “Long-term Mobile

Monitoring and Analysis of Sleep-Cognition

Relationship” from the National Science Foundation's

Smart Health and Wellbeing program to M.A.G.

Conclusions

References

Backhaus J, Born J, Hoeckesfeld R, Fokuhl S, Hohagen F, & Junghanns K (2007). Midlife decline in declarative memory consolidation is correlated with a decline in slow wave sleep . Learning & Memory , 14, 336-341.

Ellenbogen JM, Hulbert JC, Stickgold R, Dinges DF, Thompson- Schill SL (2006). Interfering with theories of sleep and memory: sleep, declarative memory, and associative interference. Current Biology , 16, 1290-1294.

Gluck MA, Myers CE (1993). Hippocampal mediation of stimulus representation: a computational theory. Hippocampus , 3, 491-516.

Lau H, Alger SE, Fishbein W (2011). Relational memory, a daytime naps facilitates abstraction of general concepts. PLoS One, 6. e27139.

Liu ZW, Faraguna U, Cirelli C, Tononi G, Gao XB (2010). Direct evidence for wake-related increases and sleep-related decreases in synaptic strength in rodent cortex. Journal of Neuroscience , 30, 8671–8675.

Moustafa AA, Myers CE, Gluck MA (2009). A neurocomputational model of classical conditioning phenomena: a putative role for the hippocampal region in associative learning. Brain Research , 1276, 180–195.

Plihal W, Born J (1997) Effects of early and late nocturnal sleep on declarative and procedural memory Journal of Cognitive Neuroscience,

9, 534–547.

Vyazovskiy VV, Cirelli C, Pfister-Genskow C, Faraguna U, Tononi G (2008). Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nature Neuroscience , 11, 2, 200–208.

Contact

Itamar Lerner, itamar.lerner@gmail.com

Mark Gluck, gluck@pavlov.rutgers.edu

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