Memory reactivation during rest is coupled with fluctuations in ongoing brain states

Poster No:

1090 

Submission Type:

Abstract Submission 

Authors:

Arielle Tambini1, Ting Xu2, Karl-Heinz Nenning1, Mark D'esposito3, Stanley Colcombe1, Michael Milham2

Institutions:

1Nathan Kline Institute, Orangeburg, NY, 2Child Mind Institute, New York, NY, 3University of California, Berkeley, CA

First Author:

Arielle Tambini  
Nathan Kline Institute
Orangeburg, NY

Co-Author(s):

Ting Xu  
Child Mind Institute
New York, NY
Karl-Heinz Nenning  
Nathan Kline Institute
Orangeburg, NY
Mark D'esposito  
University of California
Berkeley, CA
Stanley Colcombe  
Nathan Kline Institute
Orangeburg, NY
Michael Milham  
Child Mind Institute
New York, NY

Introduction:

A rich repertoire of neural dynamics is present during rest periods. One example is the reactivation of representations of past experience, a key mechanism supporting memory consolidation1. Although memory-related reactivation has been measured during rest (and sleep)2,3, it is unclear which awake brain states preferentially support reactivation. Prior work suggests a trade-off between internally-oriented brain states that promote reactivation, versus externally-focused states4-7. Recent findings support this idea, such that reactivation and related electrophysiological events coincide with default network activity, which is linked with internal processing8,9. A separate literature has characterized distinct brain states during rest via coactivation pattern (CAP) analysis10,11, which typically isolates a state reflecting internal vs. external processing (differentially weighting default vs. task-positive networks)12. Moreover, the recurring nature of CAPs is linked with slow fluctuations in global brain-wide activity (global fMRI signal, GS)13. Here, we sought to better understand which brain states support consolidation by characterizing relationships between reactivation events, brain states (i.e. CAPs), and GS fluctuations during rest.

Methods:

We analyzed an fMRI dataset (n=52), in which the reactivation of incidentally encoded object-face stimuli has been reported14. We first isolated brain states (i.e. CAPs) from the baseline (pre-encoding) rest scans (see design in Fig. 1A)10,11. To classify brain states during post-encoding rest (three 9-minute scans), the correlation between each CAP and post-encoding time point was measured and each time point was assigned to the most similar CAP. Reactivation events were defined as time points of high similarity between the encoding and post-encoding rest patterns concurrently in the hippocampus and lateral occipital cortex (LOC)14,15. Although here we characterize brain states during reactivation, the primary goal of this dataset was to test the causal role of visual cortical activity in memory consolidation, such that inhibitory Transcranial Magnetic Stimulation (TMS) was applied to LOC or a Control site after learning. As LOC TMS reduced reactivation in LOC and memory retention vs. Control conditions, here, we also tested whether TMS influenced the coupling between reactivation and CAPs.

Results:

We identified four distinct pairs of brain states (Fig. 1B). CAPs 1A and 1B captured modes of internal vs. external processing (differentially weighted default vs. dorsal attention networks). Other CAPs weighted the visual network (2A/B), the sensorimotor-association axis (3A/B), and somatomotor and ventral attention networks (4A/B). Reactivation was not uniformly distributed across CAPs (Fig. 2; F=14.5, P<10-9), but occurred preferentially during CAPs 1A and 2A, and was less likely during 1B and 3B. TMS influenced coupling between reactivation and CAPs (F=2.2, P=0.04); after LOC TMS, reactivation occurred more often during CAP 3A, and less during 2A. Moreover, reactivation tended to occur during the peak or zero phase of the GS (P<10-9, not affected by TMS). To ensure that the results were not an artifact of reactivation detection, we verified that parallel analysis of the encoding data revealed distinct coupling with CAPs.
Supporting Image: ohbm-fig1.jpg
Supporting Image: ohbm-fig2.jpg
 

Conclusions:

Memory reactivation preferentially occurred during brain states reflecting internal vs. external processing and visual activation, suggesting that promoting these brain states may facilitate (visual) memory consolidation. Modulation of these dynamics by TMS suggests that this coupling may be functionally relevant for consolidation. Our results highlight that memory reactivation is coupled with ongoing, slow fluctuations in brain states and brain-wide activity, which may reflect slow changes in other factors (e.g. arousal) that shape memory consolidation.

Brain Stimulation:

TMS

Learning and Memory:

Long-Term Memory (Episodic and Semantic) 1

Modeling and Analysis Methods:

Task-Independent and Resting-State Analysis 2

Keywords:

FUNCTIONAL MRI
Memory
Multivariate
Transcranial Magnetic Stimulation (TMS)

1|2Indicates the priority used for review

Provide references using author date format

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