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

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 agerelated 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.This research was supported by the doctoral research grants AP2009-2215 to C.S.F. and BES-2013-066842 to M.J.M.; by grants PSI2012-33625; PSI2015-65502-C2-1-P from the Spanish Ministry of Economy and Competiveness, and by the Economic Council of the Andalusian Government P08-HUM-03600-Feder and P12-CTS-2369-Feder to T.B. S.H. is supported by grants from the European Research Council (grant agreement Nº647954), the Economic and Social Research Council (ESRC grant agreement NºES/R010072/1), and the Wolfson Society and Royal Society

Two spatially distinct posterior alpha sources fulfill different functional roles in attention

Directing attention helps extracting relevant information and suppressing distracters. Alpha brain oscillations (8-12Hz) 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., 2000b), however, the effect also exists in other modalities, including the somatosensory system (Haegens et al., 2011) and inter-sensory attention tasks (Foxe and Snyder, 2011). We investigated in human participants (10 females, 10 males) the role of alpha oscillations in focused (0/100%) vs. 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, pre-stimulus alpha power in visual areas decreased linearly with increasing attention to visual stimuli. In contrast, pre-stimulus alpha power in parietal areas was lower when attention was divided between modalities/hemifields, compared to focused attention. These results suggest there are two alpha sources, where one 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

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

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

Alpha Phase Locking Predicts Residual Working Memory Performance in Schizophrenia

Background Working memory (WM) deficits are a core feature of schizophrenia. Recent electrophysiological evidence indicates that the brain systems for visual encoding are especially impaired. However, patients still achieve performance levels clearly above chance, which indicates the existence of residual mechanisms supporting WM encoding. The present study presents evidence that alpha phase locking of the electroencephalogram is a marker for such residual cognitive mechanisms. Methods Alpha phase locking during encoding into WM was compared between 17 patients with early-onset schizophrenia (EOS) and 17 healthy control subjects. Results of phase locking were correlated with accuracy. A median split based on alpha phase locking in patients was used to compare accuracy between control subjects and patients with high and low alpha phase locking. Results Alpha phase locking increased with WM memory load in both EOS and control subjects, although alpha phase locking was generally reduced in EOS. Furthermore, for EOS, a positive correlation between alpha phase locking and performance was obtained. Additionally, patients exhibiting high phase locking did not differ in performance from control subjects. Conclusions These results provide the first evidence for a relationship between alpha phase locking and visual WM encoding. This neural mechanism seems to be preserved in some patients with schizophrenia and then allows them to attain normal performance levels

The Temporal Signature of Memories: Identification of a General Mechanism for Dynamic Memory Replay in Humans

Reinstatement of dynamic memories requires the replay of neural patterns that unfold over time in a similar manner as during perception. However, little is known about the mechanisms that guide such a temporally structured replay in humans, because previous studies used either unsuitable methods or paradigms to address this question. Here, we overcome these limitations by developing a new analysis method to detect the replay of temporal patterns in a paradigm that requires participants to mentally replay short sound or video clips. We show that memory reinstatement is accompanied by a decrease of low-frequency (8 Hz) power, which carries a temporal phase signature of the replayed stimulus. These replay effects were evident in the visual as well as in the auditory domain and were localized to sensory-specific regions. These results suggest low-frequency phase to be a domain-general mechanism that orchestrates dynamic memory replay in humans

Cracking the code of oscillatory activity

Neural oscillations are ubiquitous measurements of cognitive processes and dynamic routing and gating of information. The fundamental and so far unresolved problem for neuroscience remains to understand how oscillatory activity in the brain codes information for human cognition. In a biologically relevant cognitive task, we instructed six human observers to categorize facial expressions of emotion while we measured the observers' EEG. We combined state-of-the-art stimulus control with statistical information theory analysis to quantify how the three parameters of oscillations (i.e., power, phase, and frequency) code the visual information relevant for behavior in a cognitive task. We make three points: First, we demonstrate that phase codes considerably more information (2.4 times) relating to the cognitive task than power. Second, we show that the conjunction of power and phase coding reflects detailed visual features relevant for behavioral response-that is, features of facial expressions predicted by behavior. Third, we demonstrate, in analogy to communication technology, that oscillatory frequencies in the brain multiplex the coding of visual features, increasing coding capacity. Together, our findings about the fundamental coding properties of neural oscillations will redirect the research agenda in neuroscience by establishing the differential role of frequency, phase, and amplitude in coding behaviorally relevant information in the brai

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

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

Spurious correlations in simultaneous EEG-fMRI driven by in-scanner movement

Simultaneous EEG-fMRI provides an increasingly attractive research tool to investigate cognitive processes with high temporal and spatial resolution. However, artifacts in EEG data introduced by the MR-scanner still remain a major obstacle. This study employing commonly used artifact correction steps shows that head motion, one overlooked major source of artifacts in EEG-fMRI data, can cause plausible EEG effects and EEG-BOLD correlations. Specifically, low frequency EEG

The hippocampus as the switchboard between perception and memory.

Adaptive memory recall requires a rapid and flexible switch from external perceptual reminders to internal mnemonic representations. However, owing to the limited temporal or spatial resolution of brain imaging modalities used in isolation, the hippocampal–cortical dynamics supporting this process remain unknown. We thus employed an object-scene cued recall paradigm across two studies, including intracranial electroencephalography (iEEG) and high-density scalp EEG. First, a sustained increase in hippocampal high gamma power (55 to 110 Hz) emerged 500 ms after cue onset and distinguished successful vs. unsuccessful recall. This increase in gamma power for successful recall was followed by a decrease in hippocampal alpha power (8 to 12 Hz). Intriguingly, the hippocampal gamma power increase marked the moment at which extrahippocampal activation patterns shifted from perceptual cue toward mnemonic target representations. In parallel, source-localized EEG alpha power revealed that the recall signal progresses from hippocampus to posterior parietal cortex and then to medial prefrontal cortex. Together, these results identify the hippocampus as the switchboard between perception and memory and elucidate the ensuing hippocampal–cortical dynamics supporting the recall process.post-print1844 K