scholarly journals Single-trial Phase Entrainment of Theta Oscillations in Sensory Regions Predicts Human Associative Memory Performance

2018 ◽  
Author(s):  
Danying Wang ◽  
Andrew Clouter ◽  
Qiaoyu Chen ◽  
Kimron L. Shapiro ◽  
Simon Hanslmayr

AbstractEpisodic memories are rich in sensory information and often contain integrated information from different sensory modalities. For instance, we can store memories of a recent concert with visual and auditory impressions being integrated in one episode. Theta oscillations have recently been implicated in playing a causal role synchronizing and effectively binding the different modalities together in memory. However, an open question is whether momentary fluctuations in theta synchronization predict the likelihood of associative memory formation for multisensory events. To address this question we presented movies and sounds with their luminance and volume modulated at theta (4 Hz), with a phase offset at 0° or 180° with respect to each other. This allowed us to entrain the visual and auditory cortex in a synchronous (0°) or asynchronous manner (180°). Participants were asked to remember the association between a movie and a sound while having their EEG activity recorded. Associative memory performance was significantly enhanced in the synchronous (0°) compared to the asynchronous (180°) condition. Source-level analysis demonstrated that the physical stimuli effectively entrained their respective cortical areas with a corresponding phase offset. Importantly, the strength of entrainment during encoding correlated with the efficacy of associative memory such that small phase differences between visual and auditory cortex predicted a high likelihood of correct retrieval in a later recall test. These findings suggest that theta oscillations serve a specific function in the episodic memory system: Binding the contents of different modalities into coherent memory episodes.Significance StatementHow multi-sensory experiences are bound to form a coherent episodic memory representation is one of the fundamental questions in human episodic memory research. Evidence from animal literature suggests that the relative timing between an input and theta oscillations in the hippocampus is crucial for memory formation. We precisely controlled the timing between visual and auditory stimuli and the neural oscillations at 4 Hz using a multisensory entrainment paradigm. Human associative memory formation depends on coincident timing between sensory streams processed by the corresponding brain regions. We provide evidence for a significant role of relative timing of neural theta activity in human episodic memory on a single trial level, which reveals a crucial mechanism underlying human episodic memory.

2018 ◽  
Vol 38 (28) ◽  
pp. 6299-6309 ◽  
Author(s):  
Danying Wang ◽  
Andrew Clouter ◽  
Qiaoyu Chen ◽  
Kimron L. Shapiro ◽  
Simon Hanslmayr

2017 ◽  
Author(s):  
Andrea Greve ◽  
Elisa Cooper ◽  
Roni Tibon ◽  
Richard Henson

Events that conform to our expectations, i.e, are congruent with our world knowledge or schemas, are better remembered than unrelated events. Yet events that conflict with schemas can also be remembered better. We examined this apparent paradox in four experiments, in which schemas were established by training ordinal relationships between randomly-paired objects, while episodic memory was tested for the number of objects on each trial. Better memory was found for both congruent and incongruent trials, relative to unrelated trials, producing memory performance that was a “U-shaped” function of congruency. Furthermore, the incongruency advantage, but not congruency advantage, emerged even if the information probed by the memory test was irrelevant to the schema, while the congruency advantage, but not incongruency advantage, also emerged after initial encoding. Schemas therefore augment episodic memory in multiple ways, depending on the match between novel and existing information.


2020 ◽  
Author(s):  
Srinivas Kota ◽  
Michael D. Rugg ◽  
Bradley C. Lega

1.AbstractModels of memory formation posit that recollection as compared to familiarity-based memory depends critically on the hippocampus, which binds features of an event to its context. For this reason, the contrast between study items that are later recollected versus those that are recognized on the basis of familiarity should reveal electrophysiological patterns in the hippocampus selectively involved in associative memory encoding. Extensive data from studies in rodents support a model in which theta oscillations fulfill this role, but results in humans results have not been as clear. Here, we employed an associative recognition memory procedure to identify hippocampal correlates of successful associative memory encoding and retrieval in patients undergoing intracranial EEG monitoring. We identified a dissociation between 2– 5 Hz and 5–9 Hz theta oscillations, by which 2–5 Hz oscillations uniquely were linked with successful associative memory in both the anterior and posterior hippocampus. These oscillations exhibited a significant phase reset that also predicted successful associative encoding, distinguished recollected from familiar items at retrieval, and contributed to reinstatement of encoding-related patterns that distinguished these items. Our results provide direct electrophysiological evidence that 2–5 Hz hippocampal theta oscillations support the encoding and retrieval of memories based on recollection but not familiarity.2.Significance StatementExtensive fMRI evidence suggests that the hippocampus plays a selective role in recollection rather than familiarity, during both encoding and retrieval. However, there is little or no electrophysiological evidence that speaks to whether the hippocampus is selectively involved in recollection. Here, we used intracranial EEG from human participants engaged in an associative recognition paradigm. The findings suggest that oscillatory power and phase reset in the hippocampus are selectively associated with recollection rather than familiarity-based memory judgements. Furthermore, reinstatement of oscillatory patterns in the hippocampus was stronger for successful recollection than familiarity. Collectively, the findings support a role for hippocampal theta oscillations in human episodic memory.


2020 ◽  
Vol 40 (49) ◽  
pp. 9507-9518 ◽  
Author(s):  
Srinivas Kota ◽  
Michael D. Rugg ◽  
Bradley C. Lega

2012 ◽  
Vol 1433 ◽  
pp. 98-103 ◽  
Author(s):  
Bonnie van Geldorp ◽  
Heiko C. Bergmann ◽  
Johanna Robertson ◽  
Arie J. Wester ◽  
Roy P.C. Kessels

2004 ◽  
Vol 16 (2) ◽  
pp. 178-188 ◽  
Author(s):  
Stefan Köhler ◽  
Tomáš; Paus ◽  
Randy L. Buckner ◽  
Brenda Milner

Successful recovery of words from episodic memory relies strongly on semantic processes at the time of encoding. Evidence from several functional magnetic resonance imaging (fMRI) studies has shown that changes in neural activity in the left inferior prefrontal cortex (LIPFC) during semantic encoding predict subsequent memory performance. This evidence has been taken to suggest that LIPFC plays a critical role in memory formation. Functional neuroimaging findings, however, do not establish a causal brain-behavior relationship. To determine whether there is a causal link between LIPFC involvement at encoding and subsequent success in memory performance, we conducted a two-part study in which we first used fMRI to localize encoding-related activation in LIPFC and then employed repetitive transcranial magnetic stimulation (rTMS) to manipulate neural processes in LIPFC during semantic encoding. To demonstrate the neuroanatomical specificity of any observed effect and to control for nonspecific rTMS side effects, we also stimulated neural processes in two control sites. Using frameless stereotaxy, we positioned the stimulation coil to target (1) the LIPF region that was activated during fMRI (mean xyz = −48 35 5); (2) the homologous righthemisphere region; and (3) an additional left parietal control site. At each site, “stimulated” items (600 msec of 7-Hz rTMS with Cadwell Round Coil) were intermixed with items presented without concurrent stimulation. Subsequently, subjects performed a recognition memory task for the words encountered. We found support for the predicted causal brain-behavior relationship, which was specific to LIPFC. When comparing recognition scores for stimulated items, normalized for variations in performance on nonstimulated trials, we found that words encoded under LIPFC stimulation were subsequently recognized with higher accuracy than words encoded under stimulation in the two cortical control sites. By contrast, no performance difference emerged when the two control sites were compared with each other. Based on additional analyses of the rTMS effects observed directly at the time of encoding (i.e., on semantic-decision performance), we suggest that LIPFC stimulation may have produced its effect on recognition memory, at least in part, through the triggering of more extensive processing of the stimulated items and an ensuing gain in item distinctiveness. Physiological processes of facilitation probably also contributed to the observed memory benefit. Together, these findings suggest that LIPFC does play a causal role in episodic memory formation.


Author(s):  
Benjamin J. Griffiths ◽  
María Carmen Martín-Buro ◽  
Bernhard P. Staresina ◽  
Simon Hanslmayr

AbstractEpisodic memory formation relies on at least two distinct capabilities: 1) our ability to process a vast amount of sensory information, and 2) our ability to bind these sensory representations together to form a coherent memory. The first process is thought to rely on a reduction in neocortical alpha/beta power, while the second is thought to be supported by hippocampal theta-gamma phase-amplitude coupling. However, most studies investigating human episodic memory use paradigms where the two cognitive capabilities overlap. As such, empirical support for the distinction of the two associated neural phenomena is lacking. Here, we addressed this by asking seventeen human participants (11 female, 6 male) to complete a sequence-learning paradigm that temporally separated information representation from mnemonic binding, while MEG recordings were acquired. We found that a decrease in neocortical alpha/beta power during the perception of the sequence correlated with enhanced memory performance. Similar power decreases during mnemonic binding, however, had no bearing on memory formation. In contrast, an increase in hippocampal theta/gamma phase-amplitude coupling during mnemonic binding correlated with enhanced memory performance, but similar coupling during sequence perception bared no relation to later memory performance. These results demonstrate that alpha/beta power decreases and hippocampal theta/gamma phase-amplitude coupling represent two temporally dissociable processes in episodic memory, with the former relating to information representation while the latter relates to mnemonic binding.


2020 ◽  
Author(s):  
Patrick Pruitt ◽  
Lingfei Tang ◽  
Jessica Hayes ◽  
Noa Ofen ◽  
Jessica S. Damoiseaux

Negative subsequent memory effects in functional MRI studies of memory formation, have been linked to individual differences in memory performance, yet the effect of age on this association is currently unclear. To provide insight into the brain systems related to memory across the lifespan, we examined functional neuroimaging data acquired during episodic memory formation and behavioral performance from a memory recognition task in a sample of 109 participants, including three developmental age groups (8-12, 13-17, 18-25 year-olds) and one additional group of older adults (55-85 year-olds). Young adults showed the highest memory performance and strongest negative subsequent memory effects, while older adults showed reduced negative subsequent memory effects relative to young adults. Across the sample, negative subsequent memory effects were associated with better memory performance, and there was a significant interaction between negative subsequent memory effects and memory performance by age groups. Posthoc analyses revealed that this effect was driven by a strong association between negative subsequent memory effects and memory performance in adolescents and young adults, but not in children and older adults. These findings suggest that negative subsequent memory effects may differentially support memory performance across a lifespan trajectory characterized by developmental maturation and age-related deterioration.


Sign in / Sign up

Export Citation Format

Share Document