Publications by authors named "Simon Hanslmayr"

91 Publications

Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation.

Neuroimage 2021 Nov 4;242:118454. Epub 2021 Aug 4.

School of Psychology, University of Birmingham, UK; Centre for Human Brain Health, University of Birmingham, UK; Institute for Neuroscience and Psychology, University of Glasgow, UK. Electronic address:

To form an episodic memory, we must first process a vast amount of sensory information about the to-be-encoded event and then bind these sensory representations together to form a coherent memory trace. While these two cognitive capabilities are thought to have two distinct neural origins, with neocortical alpha/beta oscillations supporting information representation and hippocampal theta-gamma phase-amplitude coupling supporting mnemonic binding, evidence for a dissociation between these two neural markers is conspicuously absent. To address this, seventeen human participants completed an associative memory task that first involved processing information about three sequentially-presented stimuli, and then binding these stimuli together into a coherent memory trace, all the while undergoing MEG recordings. We found that decreases in neocortical alpha/beta power during sequence perception, but not mnemonic binding, correlated with enhanced memory performance. Hippocampal theta/gamma phase-amplitude coupling, however, showed the opposite pattern; increases during mnemonic binding (but not sequence perception) correlated with enhanced memory performance. These results demonstrate that memory-related decreases in neocortical alpha/beta power and memory-related increases in hippocampal theta/gamma phase-amplitude coupling arise at distinct stages of the memory formation process. We speculate that this temporal dissociation reflects a functional dissociation in which neocortical alpha/beta oscillations could support the processing of incoming information relevant to the memory, while hippocampal theta-gamma phase-amplitude coupling could support the binding of this information into a coherent memory trace.
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http://dx.doi.org/10.1016/j.neuroimage.2021.118454DOI Listing
November 2021

EEG and fMRI evidence for autobiographical memory reactivation in empathy.

Hum Brain Mapp 2021 Oct 14;42(14):4448-4464. Epub 2021 Jun 14.

School of Psychology, University of Birmingham, Birmingham.

Empathy relies on the ability to mirror and to explicitly infer others' inner states. Theoretical accounts suggest that memories play a role in empathy, but direct evidence of reactivation of autobiographical memories (AM) in empathy is yet to be shown. We addressed this question in two experiments. In Experiment 1, electrophysiological activity (EEG) was recorded from 28 participants. Participants performed an empathy task in which targets for empathy were depicted in contexts for which participants either did or did not have an AM, followed by a task that explicitly required memory retrieval of the AM and non-AM contexts. The retrieval task was implemented to extract the neural fingerprints of AM and non-AM contexts, which were then used to probe data from the empathy task. An EEG pattern classifier was trained and tested across tasks and showed evidence for AM reactivation when participants were preparing their judgement in the empathy task. Participants self-reported higher empathy for people depicted in situations they had experienced themselves as compared to situations they had not experienced. A second independent fMRI experiment replicated this behavioural finding and showed increased activation for AM compared to non-AM in the brain networks underlying empathy: precuneus, posterior parietal cortex, superior and inferior parietal lobule, and superior frontal gyrus. Together, our study reports behavioural, electrophysiological, and fMRI evidence that robustly supports AM reactivation in empathy.
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http://dx.doi.org/10.1002/hbm.25557DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8410563PMC
October 2021

The Sync-Fire/deSync model: Modelling the reactivation of dynamic memories from cortical alpha oscillations.

Neuropsychologia 2021 07 24;158:107867. Epub 2021 Apr 24.

School of Psychology and Centre for Human Brain Health, University of Birmingham, UK; School of Computing, University of Kent, UK.

We propose a neural network model to explore how humans can learn and accurately retrieve temporal sequences, such as melodies, movies, or other dynamic content. We identify target memories by their neural oscillatory signatures, as shown in recent human episodic memory paradigms. Our model comprises three plausible components for the binding of temporal content, where each component imposes unique limitations on the encoding and representation of that content. A cortical component actively represents sequences through the disruption of an intrinsically generated alpha rhythm, where a desynchronisation marks information-rich operations as the literature predicts. A binding component converts each event into a discrete index, enabling repetitions through a sparse encoding of events. A timing component - consisting of an oscillatory "ticking clock" made up of hierarchical synfire chains - discretely indexes a moment in time. By encoding the absolute timing between discretised events, we show how one can use cortical desynchronisations to dynamically detect unique temporal signatures as they are reactivated in the brain. We validate this model by simulating a series of events where sequences are uniquely identifiable by analysing phasic information, as several recent EEG/MEG studies have shown. As such, we show how one can encode and retrieve complete episodic memories where the quality of such memories is modulated by the following: alpha gate keepers to content representation; binding limitations that induce a blink in temporal perception; and nested oscillations that provide preferential learning phases in order to temporally sequence events.
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http://dx.doi.org/10.1016/j.neuropsychologia.2021.107867DOI Listing
July 2021

Using fast visual rhythmic stimulation to control inter-hemispheric phase offsets in visual areas.

Neuropsychologia 2021 07 16;157:107863. Epub 2021 Apr 16.

School of Psychology, University of Birmingham, UK; Centre for Human Brain Health, University of Birmingham, UK; Institute for Neuroscience and Psychology, University of Glasgow, UK. Electronic address:

Spike timing dependent plasticity (STDP) is believed to be important for neural communication and plasticity in human episodic memory, but causal evidence is lacking due to technical challenges. Rhythmic sensory stimulation that has been used to investigate causal relations between oscillations and cognition may be able to address this question. The challenge, however, is that the frequency corresponding to the critical time window for STDP is gamma (~40 Hz), yet the application of rhythmic sensory stimulation has been limited primarily to lower frequencies (<30 Hz). It remains unknown whether this method can be applied to precisely control the activation time delay between distant groups of neurons at a millisecond scale. To answer this question and examine the role of STDP in human episodic memory, we simulated the STDP function by controlling the activation time delay between the left and right visual cortices during memory encoding. This was achieved by presenting flickering (37.5 Hz) movie pairs in the left and right visual fields with a phase lag of either 0, 90, 180 or 270°. Participants were asked to memorize the two movies within each pair and the association was later tested. Behavioral results revealed no significant difference in memory performance across conditions with different degrees of gamma phase synchrony. Yet importantly, our study showed for the first time, that oscillatory activity can be driven with a precision of 6.67 ms delay between neuronal groups. Our method hereby provides an approach to investigate relations between precise neuronal timing and cognitive functions.
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http://dx.doi.org/10.1016/j.neuropsychologia.2021.107863DOI Listing
July 2021

Alpha/beta power decreases during episodic memory formation predict the magnitude of alpha/beta power decreases during subsequent retrieval.

Neuropsychologia 2021 03 28;153:107755. Epub 2021 Jan 28.

Department of Psychology, Ludwig-Maximilians-Universität München, Munich, Germany.

Episodic memory retrieval is characterised by the vivid reinstatement of information about a personally-experienced event. Growing evidence suggests that this reinstatement is supported by reductions in the spectral power of alpha/beta activity. Given that the amount of information that can be recalled depends on the amount of information that was originally encoded, information-based accounts of alpha/beta activity would suggest that retrieval-related alpha/beta power decreases similarly depend upon decreases in alpha/beta power during encoding. To test this hypothesis, seventeen human participants completed a sequence-learning task while undergoing concurrent MEG recordings. Regression-based analyses were then used to estimate how alpha/beta power decreases during encoding predicted alpha/beta power decreases during retrieval on a trial-by-trial basis. When subjecting these parameter estimates to group-level analysis, we find evidence to suggest that retrieval-related alpha/beta (7-15Hz) power decreases fluctuate as a function of encoding-related alpha/beta power decreases. These results suggest that retrieval-related alpha/beta power decreases are contingent on the decrease in alpha/beta power that arose during encoding. Subsequent analysis uncovered no evidence to suggest that these alpha/beta power decreases reflect stimulus identity, indicating that the contingency between encoding- and retrieval-related alpha/beta power reflects the reinstatement of a neurophysiological operation, rather than neural representation, during episodic memory retrieval.
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http://dx.doi.org/10.1016/j.neuropsychologia.2021.107755DOI Listing
March 2021

Investigating the role of phase-synchrony during encoding of episodic memories using electrical stimulation.

Cortex 2020 12 29;133:37-47. Epub 2020 Sep 29.

School of Psychology, University of Birmingham, Edgbaston, Birmingham, United Kingdom; Centre for Human Brain Health, University of Birmingham, Edgbaston, Birmingham, United Kingdom; Centre for Cognitive Neuroimaging, University of Glasgow, Glasgow, United Kingdom. Electronic address:

The multi-sensory nature of episodic memories indicates that communication between a multitude of brain areas is required for their effective creation and recollection. Previous studies have suggested that the effectiveness of memory processes depends on theta synchronization (4 Hz) of sensory areas relevant to the memory. This study aimed to manipulate theta synchronization between different sensory areas in order to further test this hypothesis. We intend to entrain visual cortex with 4 Hz alternating current stimulation (tACS), while simultaneously entraining auditory cortex with 4 Hz amplitude-modulated sounds. By entraining these different sensory areas, which pertain to learned audio-visual memory associations, we expect to find that when theta is synchronized across the different sensory areas, the memory performance would be enhanced compared to when theta is not synchronized across the sensory areas. We found no evidence for such an effect in this study. It is unclear whether this is due to an inability of 4 Hz tACS to entrain the visual cortex reliably, or whether sensory entrainment is not the underlying mechanism required for episodic memory.
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http://dx.doi.org/10.1016/j.cortex.2020.09.006DOI Listing
December 2020

Entraining neurons via noninvasive electric stimulation improves cognition.

PLoS Biol 2020 10 22;18(10):e3000931. Epub 2020 Oct 22.

Institute for Neuroscience and Psychology, University of Glasgow, Glasgow, United Kingdom.

Transcranial Alternating Current Stimulation (tACS) is a method that injects rhythmic currents into the human brain via electrodes attached to the scalp of a participant. This technique allows researchers to control naturally occurring brain rhythms and study their causal relevance for cognition. Recent findings, however, cast doubts on the effectiveness of tACS to stimulate the brain and its mode of action. Two new studies by Vieira and colleagues and Marchesotti and colleagues reported in the current issue report promising new results in showing that tACS can entrain single neuron activity and improve reading abilities in dyslexic individuals.
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http://dx.doi.org/10.1371/journal.pbio.3000931DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7654821PMC
October 2020

Probing the causal involvement of dlPFC in directed forgetting using rTMS-A replication study.

PLoS One 2020 12;15(8):e0236287. Epub 2020 Aug 12.

School of Psychology, University of Birmingham, Edgbaston, Birmingham, United Kingdom.

The forgetting of previously remembered information has, for a long time, been explained by purely passive processes. This viewpoint has been challenged by the finding that humans show worse memory for specific items that they have been instructed to forget. The dorsolateral prefrontal cortex has, through imaging, lesion and brain stimulation studies, been implied in controlling such active forgetting processes. In this study, we attempted to solidify evidence for such a causal role of the dlPFC in directed forgetting by replicating an existing rTMS study (Hanslmayr S, 2012) in a preregistered within-participant design. We stimulated participants at the dlPFC (BA9) or vertex using 45s of 1Hz rTMS after instructions to forget previously remembered words in a list-method directed forgetting paradigm and tested for effects on the amount of forgotten information. Contrary to the study we were attempting to replicate, no significant increase in forgetting under dlPFC stimulation was found in our participants. However, when combining our results with the study we were attempting to replicate, dlPFC stimulation led to significantly increased directed forgetting in both studies combined. We further explored if the rTMS parameters used here and in earlier work (Hanslmayr S, 2012) influenced inhibitory processing at their time of delivery or in a more persistent manner. Unaltered incongruency and negative priming effects in a Stroop task conducted directly after stimulation suggests that our rTMS stimulation did not continue to influence inhibitory processing after the time of stimulation. As the combined evidence for increased directed forgetting due to rTMS dlPFC stimulation is still quite weak, additional replications are necessary to show that directed forgetting is indeed causally driven by an active prefrontal process.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0236287PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7423109PMC
October 2020

Memory deficits in Parkinson's disease are associated with reduced beta power modulation.

Brain Commun 2019 4;1(1):fcz040. Epub 2019 Dec 4.

School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham B15 2TT, UK.

There is an increasing recognition of the significant non-motor symptoms that burden people with Parkinson's disease. As such, there is a pressing need to better understand and investigate the mechanisms underpinning these non-motor deficits. The electrical activity within the brains of people with Parkinson's disease is known to exhibit excessive power within the beta range (12-30 Hz), compared with healthy controls. The weight of evidence suggests that this abnormally high level of beta power is the cause of bradykinesia and rigidity in Parkinson's disease. However, less is known about how the abnormal beta rhythms seen in Parkinson's disease impact on non-motor symptoms. In healthy adults, beta power decreases are necessary for successful episodic memory formation, with greater power decreases during the encoding phase predicting which words will subsequently be remembered. Given the raised levels of beta activity in people with Parkinson's disease, we hypothesized that the necessary decrease in power during memory encoding would be diminished and that this would interfere with episodic memory formation. Accordingly, we conducted a cross-sectional, laboratory-based experimental study to investigate whether there was a direct relationship between decreased beta modulation and memory formation in Parkinson's disease. Electroencephalography recordings were made during an established memory-encoding paradigm to examine brain activity in a cohort of adults with Parkinson's disease ( = 28, 20 males) and age-matched controls ( = 31, 18 males). The participants with Parkinson's disease were aged 65 ± 6 years, with an average disease duration of 6 ± 4 years, and tested on their normal medications to avoid the confound of exacerbated motor symptoms. Parkinson's disease participants showed impaired memory strength ( = 0.023) and reduced beta power decreases ( = 0.014) relative to controls. Longer disease duration was correlated with a larger reduction in beta modulation during encoding, and a concomitant reduction in memory performance. The inability to sufficiently decrease beta activity during semantic processing makes it a likely candidate to be the central neural mechanism underlying this type of memory deficit in Parkinson's disease. These novel results extend the notion that pathological beta activity is causally implicated in the motor and (lesser appreciated) non-motor deficits inherent to Parkinson's disease. These findings provide important empirical evidence that should be considered in the development of intelligent next-generation therapies.
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http://dx.doi.org/10.1093/braincomms/fcz040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7025167PMC
December 2019

Alpha/beta power decreases track the fidelity of stimulus-specific information.

Elife 2019 11 29;8. Epub 2019 Nov 29.

School of Psychology, University of Birmingham, Birmingham, United Kingdom.

Massed synchronised neuronal firing is detrimental to information processing. When networks of task-irrelevant neurons fire in unison, they mask the signal generated by task-critical neurons. On a macroscopic level, such synchronisation can contribute to alpha/beta (8-30 Hz) oscillations. Reducing the amplitude of these oscillations, therefore, may enhance information processing. Here, we test this hypothesis. Twenty-one participants completed an associative memory task while undergoing simultaneous EEG-fMRI recordings. Using representational similarity analysis, we quantified the amount of stimulus-specific information represented within the BOLD signal on every trial. When correlating this metric with concurrently-recorded alpha/beta power, we found a significant negative correlation which indicated that as post-stimulus alpha/beta power decreased, stimulus-specific information increased. Critically, we found this effect in three unique tasks: visual perception, auditory perception, and visual memory retrieval, indicating that this phenomenon transcends both stimulus modality and cognitive task. These results indicate that alpha/beta power decreases parametrically track the fidelity of both externally-presented and internally-generated stimulus-specific information represented within the cortex.
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http://dx.doi.org/10.7554/eLife.49562DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6904219PMC
November 2019

Directional coupling of slow and fast hippocampal gamma with neocortical alpha/beta oscillations in human episodic memory.

Proc Natl Acad Sci U S A 2019 10 9;116(43):21834-21842. Epub 2019 Oct 9.

School of Psychology, University of Birmingham, Birmingham B15 2TT, United Kingdom;

Episodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation. On a neural level, these 2 processes are thought to be supported by neocortical alpha/beta desynchronization and hippocampal theta/gamma synchronization, respectively. Intuitively, these 2 processes should couple to successfully create and retrieve episodic memories, yet this hypothesis has not been tested empirically. We address this by analyzing human intracranial electroencephalogram data recorded during 2 associative memory tasks. We find that neocortical alpha/beta (8 to 20 Hz) power decreases reliably precede and predict hippocampal "fast" gamma (60 to 80 Hz) power increases during episodic memory formation; during episodic memory retrieval, however, hippocampal "slow" gamma (40 to 50 Hz) power increases reliably precede and predict later neocortical alpha/beta power decreases. We speculate that this coupling reflects the flow of information from the neocortex to the hippocampus during memory formation, and hippocampal pattern completion inducing information reinstatement in the neocortex during memory retrieval.
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http://dx.doi.org/10.1073/pnas.1914180116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6815125PMC
October 2019

Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation.

PLoS Biol 2019 07 29;17(7):e3000403. Epub 2019 Jul 29.

School of Psychology, Centre for Human Brain Health, University of Birmingham, Birmingham, United Kingdom.

Decreases in low-frequency power (2-30 Hz) alongside high-frequency power increases (>40 Hz) have been demonstrated to predict successful memory formation. Parsimoniously, this change in the frequency spectrum can be explained by one factor, a change in the tilt of the power spectrum (from steep to flat) indicating engaged brain regions. A competing view is that the change in the power spectrum contains several distinct brain oscillatory fingerprints, each serving different computations. Here, we contrast these two theories in a parallel magnetoencephalography (MEG)-intracranial electroencephalography (iEEG) study in which healthy participants and epilepsy patients, respectively, studied either familiar verbal material or unfamiliar faces. We investigated whether modulations in specific frequency bands can be dissociated in time and space and by experimental manipulation. Both MEG and iEEG data show that decreases in alpha/beta power specifically predicted the encoding of words but not faces, whereas increases in gamma power and decreases in theta power predicted memory formation irrespective of material. Critically, these different oscillatory signatures of memory encoding were evident in different brain regions. Moreover, high-frequency gamma power increases occurred significantly earlier compared to low-frequency theta power decreases. These results show that simple "spectral tilt" cannot explain common oscillatory changes and demonstrate that brain oscillations in different frequency bands serve different functions for memory encoding.
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http://dx.doi.org/10.1371/journal.pbio.3000403DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6687190PMC
July 2019

Two Spatially Distinct Posterior Alpha Sources Fulfill Different Functional Roles in Attention.

J Neurosci 2019 09 24;39(36):7183-7194. Epub 2019 Jul 24.

Centre for Human Brain Health, School of Psychology, University of Birmingham, B15 2TT, Edgbaston, Birmingham, United Kingdom.

Directing attention helps to extract relevant information and suppress distracters. Alpha brain oscillations (8-12 Hz) are crucial for this process, with power decreases facilitating processing of important information and power increases inhibiting brain regions processing irrelevant information. Evidence for this phenomenon arises from visual attention studies (Worden et al., 2000); however, the effect also exists in other modalities, including the somatosensory system (Haegens et al., 2011) and intersensory attention tasks (Foxe and Snyder, 2011). We investigated in human participants (10 females, 10 males) the role of alpha oscillations in focused (0/100%) versus divided (40/60%) attention, both across modalities (visual/somatosensory; Experiment 1) and within the same modality (visual domain: across hemifields; Experiment 2) while recording EEG over 128 scalp electrodes. In Experiment 1, participants divided their attention between visual and somatosensory modality to determine the temporal/spatial frequency of a target stimulus (vibrotactile stimulus/Gabor grating). In Experiment 2, participants divided attention between two visual hemifields to identify the orientation of a Gabor grating. In both experiments, prestimulus alpha power in visual areas decreased linearly with increasing attention to visual stimuli. In contrast, prestimulus alpha power in parietal areas was lower when attention was divided between modalities/hemifields compared with focused attention. These results suggest there are two alpha sources, one of which reflects the "visual spotlight of attention" and the other reflects attentional effort. To our knowledge, this is the first study to show that attention recruits two spatially distinct alpha sources in occipital and parietal brain regions, acting simultaneously but serving different functions in attention. Attention to one spatial location/sensory modality leads to power changes of alpha oscillations (∼10 Hz) with decreased power over regions processing relevant information and power increases to actively inhibit areas processing "to-be-ignored" information. Here, we used detailed source modeling to investigate EEG data recorded during separate unimodal (visual) and multimodal (visual and somatosensory) attention tasks. Participants either focused their attention on one modality/spatial location or directed it to both. We show for the first time two distinct alpha sources are active simultaneously but play different roles. A sensory (visual) alpha source was linearly modulated by attention representing the "visual spotlight of attention." By contrast, a parietal alpha source was modulated by attentional effort, showing lowest alpha power when attention was divided.
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http://dx.doi.org/10.1523/JNEUROSCI.1993-18.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6733553PMC
September 2019

Theta oscillations show impaired interference detection in older adults during selective memory retrieval.

Sci Rep 2019 07 10;9(1):9977. Epub 2019 Jul 10.

Research Centre for Mind, Brain and Behaviour, University of Granada, Granada, Spain.

Seemingly effortless tasks, such as recognizing faces and retrieving names, become harder as we age. Such difficulties may be due to the competition generated in memory by irrelevant information that comes to mind when trying to recall a specific face or name. It is unknown, however, whether age-related struggles in retrieving these representations stem from an inability to detect competition in the first place, or from being unable to suppress competing information once interference is detected. To investigate this, we used the retrieval practice paradigm, shown to elicit memory interference, while recording electrophysiological activity in young and older adults. In two experiments, young participants showed Retrieval-Induced Forgetting (RIF), reflecting the suppression of competing information, whereas older adults did not. Neurally, mid-frontal theta power (~4-8 Hz) during the first retrieval cycle, a proxy for interference detection, increased in young compared to older adults, indicating older adults were less capable of detecting interference. Moreover, while theta power was reduced across practice cycles in younger adults, a measure of interference resolution, older adults did not show such a reduction. Thus, in contrast with younger adults, the lack of an early interference detection signal rendered older adults unable to recruit memory selection mechanisms, eliminating RIF.
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http://dx.doi.org/10.1038/s41598-019-46214-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6620337PMC
July 2019

Low-Frequency Oscillations Code Speech during Verbal Working Memory.

J Neurosci 2019 08 13;39(33):6498-6512. Epub 2019 Jun 13.

Department of Neurology, Goethe University, 60528 Frankfurt, Germany,

The way the human brain represents speech in memory is still unknown. An obvious characteristic of speech is its evolvement over time. During speech processing, neural oscillations are modulated by the temporal properties of the acoustic speech signal, but also acquired knowledge on the temporal structure of language influences speech perception-related brain activity. This suggests that speech could be represented in the temporal domain, a form of representation that the brain also uses to encode autobiographic memories. Empirical evidence for such a memory code is lacking. We investigated the nature of speech memory representations using direct cortical recordings in the left perisylvian cortex during delayed sentence reproduction in female and male patients undergoing awake tumor surgery. Our results reveal that the brain endogenously represents speech in the temporal domain. Temporal pattern similarity analyses revealed that the phase of frontotemporal low-frequency oscillations, primarily in the beta range, represents sentence identity in working memory. The positive relationship between beta power during working memory and task performance suggests that working memory representations benefit from increased phase separation. Memory is an endogenous source of information based on experience. While neural oscillations encode autobiographic memories in the temporal domain, little is known on their contribution to memory representations of human speech. Our electrocortical recordings in participants who maintain sentences in memory identify the phase of left frontotemporal beta oscillations as the most prominent information carrier of sentence identity. These observations provide evidence for a theoretical model on speech memory representations and explain why interfering with beta oscillations in the left inferior frontal cortex diminishes verbal working memory capacity. The lack of sentence identity coding at the syllabic rate suggests that sentences are represented in memory in a more abstract form compared with speech coding during speech perception and production.
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http://dx.doi.org/10.1523/JNEUROSCI.0018-19.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697399PMC
August 2019

Reactivation of neural patterns during memory reinstatement supports encoding specificity.

Cogn Neurosci 2019 Jul - Oct;10(4):175-185. Epub 2019 Jun 12.

b School of Psychology, University of Birmingham , Birmingham , UK.

Encoding specificity states that encoding and retrieving items in the same modality benefits memory, compared to encoding and retrieving in different modalities. In neural terms, this can be expressed as memory cues resonating with stored engrams; the more they overlap the better memory performance. We used temporal pattern analysis in MEG in a sensory match/mismatch memory paradigm (i.e., items presented aurally or visually) to track this resonance process. A computational model predicted that reactivation of encoding-related sensory patterns has opposing effects depending on the match or mismatch between memory cue and encoding modality. Behavioral performance was better in the match than the mismatch condition. Neural pattern reinstatement of MEG activity-benefitted memory only in the match condition, but impaired memory in the mismatch condition. These effects were only obtained for aurally but not visually encoded words. The results suggest that reactivation of encoding-related neural patterns underlies encoding specificity.
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http://dx.doi.org/10.1080/17588928.2019.1621825DOI Listing
August 2020

Modulating Human Memory via Entrainment of Brain Oscillations.

Trends Neurosci 2019 07 6;42(7):485-499. Epub 2019 Jun 6.

Department of Neurosurgery, Emory University, 1365 Clifton Road North East, Atlanta, GA 30322, USA.

In the human brain, oscillations occur during neural processes that are relevant for memory. This has been demonstrated by a plethora of studies relating memory processes to specific oscillatory signatures. Several recent studies have gone beyond such correlative approaches and provided evidence supporting the idea that modulating oscillations via frequency-specific entrainment can alter memory functions. Such causal evidence is important because it allows distinguishing mechanisms directly related to memory from mere epiphenomenal oscillatory signatures of memory. This review provides an overview of stimulation studies using different approaches to entrain brain oscillations for modulating human memory. We argue that these studies demonstrate a causal link between brain oscillations and memory, speaking against an epiphenomenal perspective of brain oscillations.
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http://dx.doi.org/10.1016/j.tins.2019.04.004DOI Listing
July 2019

Speed of time-compressed forward replay flexibly changes in human episodic memory.

Nat Hum Behav 2019 02 17;3(2):143-154. Epub 2018 Dec 17.

Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham, UK.

Remembering information from continuous past episodes is a complex task. On the one hand, we must be able to recall events in a highly accurate way, often including exact timings. On the other hand, we can ignore irrelevant details and skip to events of interest. Here, we track continuous episodes consisting of different subevents as they are recalled from memory. In behavioural and magnetoencephalography data, we show that memory replay is temporally compressed and proceeds in a forward direction. Neural replay is characterized by the reinstatement of temporal patterns from encoding. These fragments of activity reappear on a compressed timescale. Herein, the replay of subevents takes longer than the transition from one subevent to another. This identifies episodic memory replay as a dynamic process in which participants replay fragments of fine-grained temporal patterns and are able to skip flexibly across subevents.
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http://dx.doi.org/10.1038/s41562-018-0491-4DOI Listing
February 2019

Out and about: Subsequent memory effect captured in a natural outdoor environment with smartphone EEG.

Psychophysiology 2019 05 18;56(5):e13331. Epub 2019 Jan 18.

Neuropsychology Lab, Department of Psychology, European Medical School, University of Oldenburg, Oldenburg, Germany.

Spatiotemporal context plays an important role in episodic memory. While temporal context effects have been frequently studied in the laboratory, ecologically valid spatial context manipulations are difficult to implement in stationary conditions. We investigated whether the neural correlates of successful encoding (subsequent memory effect) can be captured in a real-world environment. An off-the-shelf Android smartphone was used for wireless mobile EEG acquisition and stimulus presentation. Participants encoded single words, each of which was presented at a different location on a university campus. Locations were approximately 10-12 m away from each other, half of them with striking features (landmarks) nearby. We predicted landmarks would improve recall performance. After a first free recall task of verbal stimuli indoors, participants performed a subsequent recall outdoors, in which words and locations were recalled. As predicted, significantly more words presented at landmark locations as well as significantly more landmark than nonlandmark locations were recalled. ERP analysis yielded a larger posterior positive deflection during encoding for hits compared to misses in the 400-800 ms interval. Likewise, time-frequency analysis revealed a significant difference during encoding for hits compared to misses in the form of stronger alpha (200-300 ms) and theta (300-400 ms) power increases. Our results confirm that a vibrant spatial context is beneficial in episodic memory processing and that the underlying neural correlates can be captured with unobtrusive smartphone EEG technology. The advent of mobile EEG technology promises to unveil the relevance of natural physical activity and natural environments on memory.
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http://dx.doi.org/10.1111/psyp.13331DOI Listing
May 2019

Addressing challenges of high spatial resolution UHF fMRI for group analysis of higher-order cognitive tasks: An inter-sensory task directing attention between visual and somatosensory domains.

Hum Brain Mapp 2019 03 15;40(4):1298-1316. Epub 2018 Nov 15.

Sir Peter Mansfield Imaging Centre, School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom.

Functional MRI at ultra-high field (UHF, ≥7 T) provides significant increases in BOLD contrast-to-noise ratio (CNR) compared with conventional field strength (3 T), and has been exploited for reduced field-of-view, high spatial resolution mapping of primary sensory areas. Applying these high spatial resolution methods to investigate whole brain functional responses to higher-order cognitive tasks leads to a number of challenges, in particular how to perform robust group-level statistical analyses. This study addresses these challenges using an inter-sensory cognitive task which modulates top-down attention at graded levels between the visual and somatosensory domains. At the individual level, highly focal functional activation to the task and task difficulty (modulated by attention levels) were detectable due to the high CNR at UHF. However, to assess group level effects, both anatomical and functional variability must be considered during analysis. We demonstrate the importance of surface over volume normalisation and the requirement of no spatial smoothing when assessing highly focal activity. Using novel group analysis on anatomically parcellated brain regions, we show that in higher cognitive areas (parietal and dorsal-lateral-prefrontal cortex) fMRI responses to graded attention levels were modulated quadratically, whilst in visual cortex and VIP, responses were modulated linearly. These group fMRI responses were not seen clearly using conventional second-level GLM analyses, illustrating the limitations of a conventional approach when investigating such focal responses in higher cognitive regions which are more anatomically variable. The approaches demonstrated here complement other advanced analysis methods such as multivariate pattern analysis, allowing UHF to be fully exploited in cognitive neuroscience.
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http://dx.doi.org/10.1002/hbm.24450DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6865556PMC
March 2019

An Optimal Oscillatory Phase for Pattern Reactivation during Memory Retrieval.

Curr Biol 2018 11 18;28(21):3383-3392.e6. Epub 2018 Oct 18.

School of Psychology and Centre for Human Brain Health, University of Birmingham, Birmingham B15 2TT, UK.

Computational models and in vivo studies in rodents suggest that the hippocampal system oscillates between states that are optimal for encoding and states that are optimal for retrieval. Here, we show that in humans, neural signatures of memory reactivation are modulated by the phase of a theta oscillation. Electroencephalography (EEG) was recorded while participants were cued to recall previously learned word-object associations, and time-resolved pattern classifiers were trained to detect neural reactivation of the target objects. Classifier fidelity rhythmically fluctuated at 7 or 8 Hz and was modulated by theta phase across the entire recall period. The phase of optimal classification was shifted approximately 180° between encoding and retrieval. Inspired by animal work, we then computed "classifier-locked averages" to analyze how ongoing theta oscillations behaved around the time points at which the classifier indicated memory retrieval. We found strong theta (7 or 8 Hz) phase consistency approximately 300 ms before the time points of maximal neural memory reactivation. Our findings provide important evidence that the neural signatures of memory retrieval fluctuate and are time locked to the phase of an ongoing theta oscillation.
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http://dx.doi.org/10.1016/j.cub.2018.08.065DOI Listing
November 2018

Direct Electrophysiological Evidence for Prefrontal Control of Hippocampal Processing during Voluntary Forgetting.

Curr Biol 2018 09 6;28(18):3016-3022.e4. Epub 2018 Sep 6.

Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Universitaetsstrasse 150, 44801 Bochum, Germany. Electronic address:

Forgetting does not necessarily reflect failure to encode information but can, to some extent, also be voluntarily controlled. Previous studies have suggested that voluntary forgetting relies on active inhibition of encoding processes in the hippocampus by the dorsolateral prefrontal cortex (DLPFC) [1-4]. During attentional and sensorimotor processing, enhanced DLPFC theta power alongside increased alpha/beta oscillations are a neural signature of an inhibitory top-down mechanism, with theta oscillations reflecting prefrontal control and alpha/beta oscillations occurring in areas targeted by inhibition [5-12]. Here, we used intracranial EEG recordings in presurgical epilepsy patients implanted in DLPFC (n = 13) and hippocampus (n = 15) during an item-method directed forgetting paradigm. We found that voluntary forgetting is associated with increased neural oscillations in the low theta band (3-5 Hz) in DLPFC and in a broad theta/alpha/beta (6-18 Hz) frequency range in hippocampus. Combining time-lagged correlation analysis, phase synchronization, and Granger causality in 6 patients with electrodes in both DLPFC and hippocampus, we obtained converging evidence for a top-down control of hippocampal activity by the DLPFC. Together, our results provide strong support for a model in which voluntary forgetting relies on enhanced inhibition of the hippocampus by the DLPFC.
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http://dx.doi.org/10.1016/j.cub.2018.07.042DOI Listing
September 2018

The neural dynamics of deficient memory control in heavily traumatized refugees.

Sci Rep 2018 09 3;8(1):13132. Epub 2018 Sep 3.

School of Psychology, University of Birmingham, Edgbaston, B15 2TT, Birmingham, United Kingdom.

Victims of war, torture and natural catastrophes are prone to develop posttraumatic stress disorder (PTSD). These individuals experience the recurrent, involuntary intrusion of traumatic memories. What neurocognitive mechanisms are driving this memory disorder? Here we show that PTSD symptoms in heavily traumatized refugees are related to deficits in the effective control of memory retrieval. In a think/no-think task, PTSD patients were unable to forget memories that they had previously tried to suppress when compared to control participants with the same trauma history but without PTSD. Deficits in voluntary forgetting were clinically relevant since they correlated with memory intrusions in everyday life. Magnetoencephalography (MEG) recorded during suppression attempts revealed that PTSD patients were unable to downregulate signatures of sensory long-term memory traces in the gamma frequency band (70-120 Hz). Thus, our data suggest that the inability to suppress unwanted memories through modulation of gamma activity is related to PTSD symptom severity.
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http://dx.doi.org/10.1038/s41598-018-31400-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6120867PMC
September 2018

Replay of Stimulus-specific Temporal Patterns during Associative Memory Formation.

J Cogn Neurosci 2018 11 13;30(11):1577-1589. Epub 2018 Jul 13.

University of Birmingham.

Forming a memory often entails the association of recent experience with present events. This recent experience is usually an information-rich and dynamic representation of the world around us. We here show that associating a static cue with a previously shown dynamic stimulus yields a detectable, dynamic representation of this stimulus. We further implicate this representation in the decrease of low-frequency power (∼4-30 Hz) in the ongoing EEG, which is a well-known correlate of successful memory formation. The reappearance of content-specific patterns in desynchronizing brain oscillations was observed in two sensory domains, that is, in a visual condition and in an auditory condition. Together with previous results, these data suggest a mechanism that generalizes across domains and processes, in which the decrease in oscillatory power allows for the dynamic representation of information in ongoing brain oscillations.
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http://dx.doi.org/10.1162/jocn_a_01304DOI Listing
November 2018

Data-driven re-referencing of intracranial EEG based on independent component analysis (ICA).

J Neurosci Methods 2018 09 28;307:125-137. Epub 2018 Jun 28.

School of Psychology, University of Birmingham, UK; Centre for Human Brain Health, University of Birmingham, UK. Electronic address:

Background: Intracranial recordings from patients implanted with depth electrodes are a valuable source of information in neuroscience. They allow for the unique opportunity to record brain activity with high spatial and temporal resolution. A common pre-processing choice in stereotactic EEG (S-EEG) is to re-reference the data with a bipolar montage. In this, each channel is subtracted from its neighbor, to reduce commonalities between channels and isolate activity that is spatially confined.

New Method: We challenge the assumption that bipolar reference effectively performs this task. To extract local activity, the distribution of the signal source of interest, interfering distant signals, and noise need to be considered. Referencing schemes with fixed coefficients can decrease the signal to noise ratio (SNR) of the data, they can lead to mislocalization of activity and consequently to misinterpretation of results. We propose to use Independent Component Analysis (ICA), to derive filter coefficients that reflect the statistical dependencies of the data at hand.

Results: We describe and demonstrate this on human S-EEG recordings. In a simulation with real data, we quantitatively show that ICA outperforms the bipolar referencing operation in sensitivity and importantly in specificity when revealing local time series from the superposition of neighboring channels.

Comparison With Existing Method(s): We argue that ICA already performs the same task that bipolar referencing pursues, namely undoing the linear superposition of activity and will identify activity that is local.

Conclusions: When investigating local sources in human S-EEG, ICA should be preferred over re-referencing the data with a bipolar montage.
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http://dx.doi.org/10.1016/j.jneumeth.2018.06.021DOI Listing
September 2018

Single-Trial Phase Entrainment of Theta Oscillations in Sensory Regions Predicts Human Associative Memory Performance.

J Neurosci 2018 07 13;38(28):6299-6309. Epub 2018 Jun 13.

School of Psychology, Centre for Human Brain Health, University of Birmingham, Birmingham B15 2TT, United Kingdom

Episodic 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 entrained the visual and auditory cortex at theta frequency (4 Hz) and in a synchronous or asynchronous manner by modulating the luminance and volume of movies and sounds at 4 Hz, with a phase offset at 0° or 180°. EEG activity from human subjects (both sexes) was recorded while they memorized the association between a movie and a sound. Associative memory performance was significantly enhanced in the 0° compared with the 180° condition. Source-level analysis demonstrated that the physical stimuli effectively entrained their respective cortical areas with a corresponding phase offset. The findings suggested a successful replication of a previous study (Clouter et al., 2017). 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. How multisensory 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.
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http://dx.doi.org/10.1523/JNEUROSCI.0349-18.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6596103PMC
July 2018

Across-subjects classification of stimulus modality from human MEG high frequency activity.

PLoS Comput Biol 2018 03 12;14(3):e1005938. Epub 2018 Mar 12.

Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands.

Single-trial analyses have the potential to uncover meaningful brain dynamics that are obscured when averaging across trials. However, low signal-to-noise ratio (SNR) can impede the use of single-trial analyses and decoding methods. In this study, we investigate the applicability of a single-trial approach to decode stimulus modality from magnetoencephalographic (MEG) high frequency activity. In order to classify the auditory versus visual presentation of words, we combine beamformer source reconstruction with the random forest classification method. To enable group level inference, the classification is embedded in an across-subjects framework. We show that single-trial gamma SNR allows for good classification performance (accuracy across subjects: 66.44%). This implies that the characteristics of high frequency activity have a high consistency across trials and subjects. The random forest classifier assigned informational value to activity in both auditory and visual cortex with high spatial specificity. Across time, gamma power was most informative during stimulus presentation. Among all frequency bands, the 75 Hz to 95 Hz band was the most informative frequency band in visual as well as in auditory areas. Especially in visual areas, a broad range of gamma frequencies (55 Hz to 125 Hz) contributed to the successful classification. Thus, we demonstrate the feasibility of single-trial approaches for decoding the stimulus modality across subjects from high frequency activity and describe the discriminative gamma activity in time, frequency, and space.
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http://dx.doi.org/10.1371/journal.pcbi.1005938DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5864083PMC
March 2018

The Sync/deSync Model: How a Synchronized Hippocampus and a Desynchronized Neocortex Code Memories.

J Neurosci 2018 04 27;38(14):3428-3440. Epub 2018 Feb 27.

School of Computing, University of Kent, Canterbury CT2 7NF, United Kingdom and.

Neural oscillations are important for memory formation in the brain. The desynchronization of alpha (10 Hz) oscillations in the neocortex has been shown to predict successful memory encoding and retrieval. However, when engaging in learning, it has been found that the hippocampus synchronizes in theta (4 Hz) oscillations, and that learning is dependent on the phase of theta. This inconsistency as to whether synchronization is "good" for memory formation leads to confusion over which oscillations we should expect to see and where during learning paradigm experiments. This paper seeks to respond to this inconsistency by presenting a neural network model of how a well functioning learning system could exhibit both of these phenomena, i.e., desynchronization of alpha and synchronization of theta during successful memory encoding.We present a spiking neural network (the Sync/deSync model) of the neocortical and hippocampal system. The simulated hippocampus learns through an adapted spike-time dependent plasticity rule, in which weight change is modulated by the phase of an extrinsically generated theta oscillation. Additionally, a global passive weight decay is incorporated, which is also modulated by theta phase. In this way, the Sync/deSync model exhibits theta phase-dependent long-term potentiation and long-term depression. We simulated a learning paradigm experiment and compared the oscillatory dynamics of our model with those observed in single-cell and scalp-EEG studies of the medial temporal lobe. Our Sync/deSync model suggests that both the desynchronization of neocortical alpha and the synchronization of hippocampal theta are necessary for successful memory encoding and retrieval. A fundamental question is the role of rhythmic activation of neurons, i.e., how and why their firing oscillates between high and low rates. A particularly important question is how oscillatory dynamics between the neocortex and hippocampus support memory formation. We present a spiking neural-network model of such memory formation, with the central ideas that (1) in neocortex, neurons need to break out of an alpha oscillation to represent a stimulus (i.e., alpha desynchronizes), whereas (2) in hippocampus, the firing of neurons at theta facilitates formation of memories (i.e., theta synchronizes). Accordingly, successful memory formation is marked by reduced neocortical alpha and increased hippocampal theta. This pattern has been observed experimentally and gives our model its name-the Sync/deSync model.
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http://dx.doi.org/10.1523/JNEUROSCI.2561-17.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6596040PMC
April 2018

Theta Phase Synchronization Is the Glue that Binds Human Associative Memory.

Curr Biol 2017 Oct 5;27(20):3143-3148.e6. Epub 2017 Oct 5.

School of Psychology, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK. Electronic address:

Episodic memories are information-rich, often multisensory events that rely on binding different elements [1]. The elements that will constitute a memory episode are processed in specialized but distinct brain modules. The binding of these elements is most likely mediated by fast-acting long-term potentiation (LTP), which relies on the precise timing of neural activity [2]. Theta oscillations in the hippocampus orchestrate such timing as demonstrated by animal studies in vitro [3, 4] and in vivo [5, 6], suggesting a causal role of theta activity for the formation of complex memory episodes, but direct evidence from humans is missing. Here, we show that human episodic memory formation depends on phase synchrony between different sensory cortices at the theta frequency. By modulating the luminance of visual stimuli and the amplitude of auditory stimuli, we directly manipulated the degree of phase synchrony between visual and auditory cortices. Memory for sound-movie associations was significantly better when the stimuli were presented in phase compared to out of phase. This effect was specific to theta (4 Hz) and did not occur in slower (1.7 Hz) or faster (10.5 Hz) frequencies. These findings provide the first direct evidence that episodic memory formation in humans relies on a theta-specific synchronization mechanism.
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http://dx.doi.org/10.1016/j.cub.2017.09.001DOI Listing
October 2017

Human Memory: Brain-State-Dependent Effects of Stimulation.

Curr Biol 2017 05;27(10):R385-R387

School of Psychology, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK. Electronic address:

A new study shows that direct stimulation of memory-relevant brain areas can enhance memory performance, but only when stimulation is applied during brain states associated with poor memory outcome - stimulation during optimal states results in a decrease in memory.
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http://dx.doi.org/10.1016/j.cub.2017.03.079DOI Listing
May 2017
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