Alpha oscillations during incidental encoding predict subsequent memory for new “foil” information

Vogelsang, David A.; Gruber, Matthias J.; Bergström, Zara M.; Ranganath, Charan; Simons, Jon S.

doi:10.1101/141648

Cited by 8 publications

(9 citation statements)

References 61 publications

(98 reference statements)

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“…Despite the long history of M/EEG studies on recognition memory (Sanquist et al, 1980; for reviews, see Mecklinger, 2000; Rugg and Curran, 2007), only a few have examined oscillatory patterns related to different memory outcomes (Burgess & Gruzelier, 2000; Khader & Rösler, 2011; Michelmann, Bowman, & Hanslmayr, 2016; Vogelsang, Gruber, Bergström, Ranganath, & Simons, 2018; Waldhauser, Braun, & Hanslmayr, 2016), albeit without explicitly distinguishing associative recall from item recognition. Our current paradigm allowed us to directly probe the oscillatory mechanisms that support these different memory signals (Figure 1).…”

Section: Resultsmentioning

confidence: 99%

Alpha rhythms reveal when, where and how memories are retrieved

Martín-Buro

Wimber

Henson

et al. 2019

Preprint

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SummaryOur memories for past experiences can range from vague recognition to full-blown recall of associated details. Neuroimaging research has tried to understand the brain mechanisms underlying qualitatively different memories for decades (Yonelinas, 2002). On the one hand, Electroencephalography (EEG) has shown that recall signals unfold a few hundred milliseconds after simple recognition and are hallmarked by sustained voltage deflections over left posterior sensors (Herron, 2007; Johansson & Mecklinger, 2003; Mecklinger, Rosburg, & Johansson, 2016; Rugg & Curran, 2007). However, sensor-based analyses only provide limited insights into the supporting brain networks. On the other hand, functional magnetic resonance imaging (fMRI) has revealed a ‘core recollection network’ centred on posterior parietal and medial temporal lobe (MTL) regions (Hayama, Vilberg, & Rugg, 2012; Johnson, Suzuki, & Rugg, 2013; King, de Chastelaine, Elward, Wang, & Rugg, 2015; Rugg, Johnson, & Uncapher, 2015; Rugg & Vilberg, 2013; Thakral, Benoit, & Schacter, 2017). However, due to the relatively poor time resolution of fMRI, the temporal dynamics of these regions during retrieval remain largely unknown. In order to overcome these modality-specific limitations, we here used Magnetoencephalography (MEG) in a verbal episodic memory paradigm assessing correct rejection (CR) of lures, item recognition (IR) of old words and associative recall (AR) of paired target words. We found that power decreases in the alpha frequency band (10-12 Hz) systematically track different mnemonic outcomes in both time and space: Over left posterior sensors, alpha power decreased in a stepwise fashion from 500 ms onward, first from CR to IR and then from IR to AR. When projecting alpha power into source space, the ‘core recollection network’ known from fMRI studies emerged, including posterior parietal cortex (PPC) and hippocampus. While PPC showed a linear change across conditions, hippocampal effects were specific to recall. Critically, the hippocampal recall effect emerged ∼200 ms before the PPC recall effect, suggesting a bottom-up recall signal from hippocampus to PPC. Our data thus link engagement of the core recollection network to the temporal dynamics of episodic memory and suggest that alpha rhythms constitute a fundamental oscillatory mechanism revealing when, where and how our memories are retrieved.HighlightsAlpha rhythms distinguish between different retrieval outcomesAlpha power time courses track item recognition and associative recallSource alpha power decreases track the fMRI core recollection networkHippocampal recall signal precedes parietal signal

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Section: Resultsmentioning

confidence: 99%

Alpha rhythms reveal when, where and how memories are retrieved

Martín-Buro

Wimber

Henson

et al. 2019

Preprint

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“…This strategy thus involves focusing on semantic aspects of stimuli ("deep" processing) in a recognition test if the initial encoding task involved semantic judgements, versus focusing on perceptual aspects of stimuli ("shallow" processing) if the initial encoding task involved perceptual judgements. By reinstating such different processing modes, the foils become more deeply encoded in the deep test than the shallow test (see Danckert, et al, 2011;Gray & Gallo, 2015;Jacoby, Shimizu, Daniels, et al, 2005;Vogelsang et al, 2016Vogelsang et al, , 2018.…”

Section: Discussionmentioning

confidence: 99%

“…The experiment was programmed and run in PsychoPy (Peirce et al, 2019;Peirce, 2007) on a tablet computer. In total 288 English words from the MRC psycholinguistic database (Wilson, 1988) were used as stimuli (3-11 characters, Kucera-Francis frequency range 0-591), drawn from a larger set used by Vogelsang et al (2016Vogelsang et al ( , 2018. The words were randomly split into twelve lists of 24 words each, with assignment to experimental conditions counterbalanced across participants (see procedure for details).…”

Section: Methodsmentioning

confidence: 99%

“…Evidence that participants spontaneously constrain retrieval in this way comes from the "memory-for-foils" paradigm (Jacoby, Shimizu, Daniels, et al, 2005). In the most relevant version of this paradigm (Vogelsang, Bonnici, Bergström, Ranganath, & Simons, 2016;Vogelsang, Gruber, Bergström, Ranganath, & Simons, 2018), participants first encode two different word lists in two different encoding tasks. The first task encourages participants to focus on the meaning of the words by rating them for pleasantness (considered "deep", semantically-oriented processing in the Levels of Processing (LOP) framework; Craik & Lockhart, 1972).…”

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confidence: 99%

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Intact strategic retrieval processes in older adults: no evidence for age-related deficits in source-constrained retrieval

Salhi

Bergström

2020

Memory

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Aging is thought to involve impairments to cognitive control functions that support episodic memory, for example by enabling people to strategically constrain their retrieval search towards a specific context ("source") in order to facilitate retrieval of goal-relevant memories. The "memory-for-foils" paradigm investigates source-constrained retrieval by assessing whether incidental encoding of new foils during an old/new recognition test differs depending on the type of processing that was previously used during study of the old items in the test. If it does, it suggests that people process foils differently as a result of engaging in source-constrained retrieval attempts. Young adults typically show differences in incidental encoding foils, but such differences have not been found in older adults. Here, we compared source-constrained retrieval and reward effects on incidental foil encoding between younger and older adults, to assess if age-related reductions in strategic retrieval processing are accompanied by differences in responsiveness to external rewards. The results showed only minor effects of rewards on memory processing, in younger adults only. Contrary to prior findings, older adults had equivalent overall memory performance and spontaneously constrained retrieval to the same extent as the young group, showing that aging-related impairments to strategic retrieval processes are not inevitable.

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“…Furthermore, previous studies have shown that encoding-related brain activity (i.e., predictive of subsequent memory) is shaped both by the type of processing occurring at encoding and by the overlap between encoding and retrieval processes (Bauch and Otten, 2012; Fellner et al, 2013; Staudigl and Hanslmayr, 2013; Vogelsang et al, 2016; 2018; Long and Kahana, 2017). The typical procedure in these previous studies has been to investigate encoding-related brain activity when explicitly instructing participants to attend to particular attributes during the encoding and retrieval.…”

Section: Introductionmentioning

confidence: 99%

Neural Pattern Classification Tracks Transfer-Appropriate Processing in Episodic Memory

Bramão

Johansson

2018

eNeuro

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The transfer-appropriate processing (TAP) account holds that episodic memory depends on the overlap between encoding and retrieval processing. In the current study, we employed multivariate pattern analysis (MVPA) of electroencephalography to examine the relevance of spontaneously engaged visual processing during encoding for later retrieval. Human participants encoded word-picture associations, where the picture could be a famous face, a landmark, or an object. At test, we manipulated the retrieval demands by asking participants to retrieve either visual or verbal information about the pictures. MVPA revealed classification between picture categories during early perceptual stages of encoding (∼170 ms). Importantly, these visual category-specific neural patterns were predictive of later episodic remembering, but the direction of the relationship was contingent on the particular retrieval demand of the memory task: a benefit for the visual and a cost for the verbal. A reinstatement of the category-specific neural patterns established during encoding was observed during retrieval, and again the relationship with behavior varied with retrieval demands. Reactivation of visual representations during retrieval was associated with better memory in the visual task, but with lower performance in the verbal task. Our findings support and extend the TAP account by demonstrating that processing of particular aspects during memory formation can also have detrimental effects on later episodic remembering when other aspects of the event are called-for and shed new light on encoding and retrieval interactions in episodic memory.

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Alpha oscillations during incidental encoding predict subsequent memory for new “foil” information

Cited by 8 publications

References 61 publications

Alpha rhythms reveal when, where and how memories are retrieved

Alpha rhythms reveal when, where and how memories are retrieved

Intact strategic retrieval processes in older adults: no evidence for age-related deficits in source-constrained retrieval

Neural Pattern Classification Tracks Transfer-Appropriate Processing in Episodic Memory

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