Blocking of irrelevant memories by posterior alpha activity boosts memory encoding

In our daily lives, we are confronted with a large amount of information. Because only a small fraction can be encoded in long‐term memory, the brain must rely on powerful mechanisms to filter out irrelevant information. To understand the neuronal mechanisms underlying the gating of information into long‐term memory, we employed a paradigm where the encoding was directed by a “Remember” or a “No‐Remember” cue. We found that posterior alpha activity increased prior to the “No‐Remember” stimuli, whereas it decreased prior to the “Remember” stimuli. The sources were localized in the parietal cortex included in the dorsal attention network. Subjects with a larger cue‐modulation of the alpha activity had better memory for the to‐be‐remembered items. Interestingly, alpha activity reflecting successful inhibition following the “No‐Remember” cue was observed in the frontal midline structures suggesting preparatory inhibition was mediated by anterior parts of the dorsal attention network. During the presentation of the memory items, there was more gamma activity for the “Remember” compared to the “No‐Remember” items in the same regions. Importantly, the anticipatory alpha power during cue predicted the gamma power during item. Our findings suggest that top‐down controlled alpha activity reflects attentional inhibition of sensory processing in the dorsal attention network, which then finally gates information to long‐term memory. This gating is achieved by inhibiting the processing of visual information reflected by neuronal synchronization in the gamma band. In conclusion, the functional architecture revealed by region‐specific changes in the alpha activity reflects attentional modulation which has consequences for long‐term memory encoding. Hum Brain Mapp 35:3972–3987, 2013. © 2013 Wiley Periodicals, Inc.     

Load effects on spatial working memory performance are linked to distributed alpha and beta oscillations

Increasing spatial working memory (SWM) load is generally associated with declines in behavioral performance, but the neural correlates of load‐related behavioral effects remain poorly understood. Herein, we examine the alterations in oscillatory activity that accompany such performance changes in 22 healthy adults who performed a two‐ and four‐load SWM task during magnetoencephalography (MEG). All MEG data were transformed into the time‐frequency domain and significant oscillatory responses were imaged separately per load using a beamformer. Whole‐brain correlation maps were computed using the load‐related beamformer difference images and load‐related accuracy effects on the SWM task. The results indicated that load‐related differences in left inferior frontal alpha activity during encoding and maintenance were negatively correlated with load‐related accuracy differences on the SWM task. That is, individuals who had more substantial decreases in prefrontal alpha during high‐relative to low‐load SWM trials tended to have smaller performance decrements on the high‐load condition (i.e., they performed more accurately). The same pattern of neurobehavioral correlations was observed during the maintenance period for right superior temporal alpha activity and right superior parietal beta activity. Importantly, this is the first study to employ a voxel‐wise whole‐brain approach to significantly link load‐related oscillatory differences and load‐related SWM performance differences.     

Increase in posterior alpha activity during rehearsal predicts successful long-term memory formation of word sequences

It is becoming increasingly clear that demanding cognitive tasks rely on an extended network engaging task-relevant areas and, importantly, disengaging task-irrelevant areas. Given that alpha activity (8-12 Hz) has been shown to reflect the disengagement of task-irrelevant regions in attention and working memory tasks, we here ask if alpha activity plays a related role for long-term memory formation. Subjects were instructed to encode and maintain the order of word sequences while the ongoing brain activity was recorded using magnetoencephalography (MEG). In each trial, three words were presented followed by a 3.4 s rehearsal interval. Considering the good temporal resolution of MEG this allowed us to investigate the word presentation and rehearsal interval separately. The sequences were grouped in trials where word order either could be tested immediately (working memory trials; WM) or later (LTM trials) according to instructions. Subjects were tested on their ability to retrieve the order of the three words. The data revealed that alpha power in parieto-occipital regions was lower during word presentation compared to rehearsal. Our key finding was that parieto-occipital alpha power during the rehearsal period was markedly stronger for successfully than unsuccessfully encoded LTM sequences. This subsequent memory effect demonstrates that high posterior alpha activity creates an optimal brain state for successful LTM formation possibly by actively reducing parieto-occipital activity that might interfere with sequence encoding.     

Effortful verb retrieval from semantic memory drives beta suppression in mesial frontal regions involved in action initiation

The contribution of the motor cortex to the semantic retrieval of verbs remains a subject of debate in neuroscience. Here, we examined whether additional engagement of the cortical motor system was required when access to verbs semantics was hindered during a verb generation task. We asked participants to produce verbs related to presented noun cues that were either strongly associated with a single verb to prompt fast and effortless verb retrieval, or were weakly associated with multiple verbs and more difficult to respond to. Using power suppression of magnetoencephalography beta oscillations (15–30 Hz) as an index of cortical activation, we performed a whole‐brain analysis in order to identify the cortical regions sensitive to the difficulty of verb semantic retrieval. Highly reliable suppression of beta oscillations occurred 250 ms after the noun cue presentation and was sustained until the onset of verbal response. This was localized to multiple cortical regions, mainly in the temporal and frontal lobes of the left hemisphere. Crucially, the only cortical regions where beta suppression was sensitive to the task difficulty, were the higher order motor areas on the medial and lateral surfaces of the frontal lobe. Stronger activation of the premotor cortex and supplementary motor area accompanied the effortful verb retrieval and preceded the preparation of verbal responses for more than 500 ms, thus, overlapping with the time window of verb retrieval from semantic memory. Our results suggest that reactivation of verb‐related motor plans in higher order motor circuitry promotes the semantic retrieval of target verbs.     

Dissociation between MEG alpha modulation and performance accuracy on visual working memory task in obsessive compulsive disorder

Oscillatory brain activity in the alpha band (8-13 Hz) is modulated by cognitive events. Such modulation is reflected in a decrease of alpha (event-related desynchronization; ERD) with high cognitive load, or an increase (event-related synchronization) with low cognitive demand or with active inhibition of distractors. We used magnetoencephalography to investigate the pattern of prefrontal and parieto-occipital alpha modulation related to two variants of visual working memory task (delayed matching-to-sample) with and without a distractor. We tested nonmedicated, nondepressed patients suffering obsessive-compulsive disorder (OCD), and pair-matched healthy controls. The level of event-related alpha as a function of time was estimated using the temporal-spectral evolution technique. The results in OCD patients indicated: (1) a lower level of prestimulus (reference) alpha when compared to controls, (2) a task-phase specific reduction in event-related alpha ERD in particular for delayed matching-to-sample task with distractor, (3) no significant correlations between the pattern of modulation in prefrontal and parietal-occipital alpha oscillatory activity. Despite showing an abnormally low alpha modulation, the OCD patients' performance accuracy was normal. The results suggest a relationship of alpha oscillations and the underlying thalamocortical network to etiology of OCD and an involvement of a compensatory mechanism related to effortful inhibition of extrinsic and intrinsic interference.     

Dynamic links between theta executive functions and alpha storage buffers in auditory and visual working memory

Working memory (WM) tasks require not only distinct functions such as a storage buffer and central executive functions, but also coordination among these functions. Neuroimaging studies have revealed the contributions of different brain regions to different functional roles in WM tasks; however, little is known about the neural mechanism governing their coordination. Electroencephalographic (EEG) rhythms, especially theta and alpha, are known to appear over distributed brain regions during WM tasks, but the rhythms associated with task‐relevant regional coupling have not been obtained thus far. In this study, we conducted time–frequency analyses for EEG data in WM tasks that include manipulation periods and memory storage buffer periods. We used both auditory WM tasks and visual WM tasks. The results successfully demonstrated function‐specific EEG activities. The frontal theta amplitudes increased during the manipulation periods of both tasks. The alpha amplitudes increased during not only the manipulation but also the maintenance periods in the temporal area for the auditory WM and the parietal area for the visual WM. The phase synchronization analyses indicated that, under the relevant task conditions, the temporal and parietal regions show enhanced phase synchronization in the theta bands with the frontal region, whereas phase synchronization between theta and alpha is significantly enhanced only within the individual areas. Our results suggest that WM task‐relevant brain regions are coordinated by distant theta synchronization for central executive functions, by local alpha synchronization for the memory storage buffer, and by theta–alpha coupling for inter‐functional integration.     

EEG alpha synchronization and functional coupling during top-down processing in a working memory task

Electroencephalogram (EEG) alpha (around 10 Hz) is the dominant rhythm in the human brain during conditions of mental inactivity. High amplitudes as observed during rest usually diminish during cognitive effort. During retention of information in working memory, however, power increase of alpha oscillations can be observed. This alpha synchronization has been interpreted as cortical idling or active inhibition. The present study provides evidence that during top-down processing in a working memory task, alpha power increases at prefrontal but decreases at occipital electrode sites, thereby reaching a state in which alpha power and frequency become very similar over large distances. Two experimental conditions were compared. In the first, visuospatial information only had to be retained in memory whereas the second condition additionally demanded manipulation of the information. During the second condition, stronger alpha synchronization at prefrontal sites and larger occipital alpha suppression was observed as compared to that for pure retention. This effect was accompanied by assimilation of prefrontal and occipital alpha frequency, stronger functional coupling between prefrontal and occipital brain areas, and alpha latency shifts from prefrontal cortex to primary visual areas, possibly indicating the control of posterior cortical activation by anterior brain areas. An increase of prefrontal EEG alpha amplitudes, which is accompanied by a decrease at posterior sites, thus may not be interpreted in terms of idling or "global" inhibition but may enable a tight functional coupling between prefrontal cortical areas, and thereby allows the control of the execution of processes in primary visual brain regions.     

Magnetic oscillatory responses to lateralization changes of natural and artificial sounds in humans

Oscillatory signals in human magnetoencephalogram were investigated as correlates of cortical network activity in response to sound lateralization changes. Previously, we found lateralized presentations of a monosyllabic word to elicit posterior temporo-parietal gamma-band activity, possibly reflecting synchronization of neuronal assemblies in putative auditory dorsal stream areas. In addition, beta activity was decreased over sensorimotor regions, suggesting the activation of motor networks involved in orientating. The present study investigated responses to lateralization changes of both a barking dog sound and a distorted noise to test whether beta desynchronization would depend on the sound's relevance for orientating. Eighteen adults listened passively to 900 samples of each sound in separate location mismatch paradigms with midline standards and both right- and left-lateralized deviants. Lateralized distorted noises were accompanied by enhanced spectral amplitude at 58-73 Hz over right temporo-parietal cortex. Left-lateralized barking dog sounds elicited right and right-lateralized sounds elicited bilateral temporo-parietal spectral amplitude increases at approximately 77 Hz. This replicated the involvement of posterior temporo-parietal areas in auditory spatial processing. Only barking dog sounds, but not distorted noises, gave rise to 30 Hz desynchronization over contralateral sensorimotor areas, parieto-frontal gamma coherence increases and beta coherence reductions between sensorimotor and prefrontal sensors. Apparently passive listening to lateralized natural sounds with a potential biological relevance led to an activation of motor networks involved in the automatic preparation for orientating. Parieto-frontal coherence increases may reflect enhanced coupling of networks involved in the integration of auditory spatial and motor processes.     

Dissociation between phase‐locked and nonphase‐locked alpha oscillations in a working memory task

The functions of human alpha oscillations (～10 Hz) were related to cognitive processes such as memory and top‐down control. Recent models suggest that alpha phase serves as a mechanism especially relevant for the timing of neural activity, whereas alpha amplitude is important for the inhibition of task‐irrelevant brain areas. This study investigates directly the influence of top‐down modulation on phase‐locked and nonphase‐locked alpha rhythms. We conducted an EEG experiment where subjects performed a working memory task. In the encoding phase of the task subjects had to learn presented pictures of nonliving objects that could later be asked to be retrieved. We varied the top‐down modulation by including cues indicating either to remember or to forget (not to remember) the next following item. Spectral analyses showed that nonremember cues elicited pronounced alpha amplitude increase compared to remember cues. Furthermore, phase‐locking in low frequencies, especially in the alpha range (7–12 Hz), was stronger for remember as opposed to not‐to‐remember items. In conclusion, we propose that alpha amplitude reflects top‐down modulated inhibition and that alpha phase is important for the exact timing of neural activity and can be related to binding processes. Hum Brain Mapp, 2009. © 2009 Wiley‐Liss, Inc.     

Emotion perception and executive control interact in the salience network during emotionally charged working memory processing

Processing of emotional stimuli can either hinder or facilitate ongoing working memory (WM); however, the neural basis of these effects remains largely unknown. Here we examined the neural mechanisms of these paradoxical effects by implementing a novel emotional WM task in an fMRI study. Twenty‐five young healthy participants performed an N‐back task with fearful and neutral faces as stimuli. Participants made more errors when performing 0‐back task with fearful versus neutral faces, whereas they made fewer errors when performing 2‐back task with fearful versus neutral faces. These emotional impairment and enhancement on behavioral performance paralleled significant interactions in distributed regions in the salience network including anterior insula (AI) and dorsal cingulate cortex (dACC), as well as in emotion perception network including amygdala and temporal‐occipital association cortex (TOC). The dorsal AI (dAI) and dACC were more activated when comparing fearful with neutral faces in 0‐back task. Contrarily, dAI showed reduced activation, while TOC and amygdala showed stronger responses to fearful as compared to neutral faces in the 2‐back task. These findings provide direct neural evidence to the emerging dual competition model suggesting that the salience network plays a critical role in mediating interaction between emotion perception and executive control when facing ever‐changing behavioral demands. Hum Brain Mapp 35:5606–5616, 2014. © 2014 Wiley Periodicals, Inc.     

Spatio-temporal dynamics of working memory maintenance and scanning of verbal information

ObjectiveDuring verbal communication, humans briefly maintain mental representations of speech sounds conveying verbal information, and constantly scan these representations for comparison to incoming information. We determined the spatio-temporal dynamics of such short-term maintenance and subsequent scanning of verbal information, by intracranially measuring high-gamma activity at 70–110 Hz during a working memory task.MethodsPatients listened to a stimulus set of two or four spoken letters and were instructed to remember those letters over a two-second interval, following which they were asked to determine if a subsequent target letter had been presented earlier in that trial’s stimulus set.ResultsAuditory presentation of letter stimuli sequentially elicited high-gamma augmentation bilaterally in the superior-temporal and pre-central gyri. During the two-second maintenance period, high-gamma activity was augmented in the left pre-central gyrus, and this effect was larger during the maintenance of stimulus sets consisting of four compared to two letters. During the scanning period following target presentation, high-gamma augmentation involved the left inferior-frontal and supra-marginal gyri.ConclusionsShort-term maintenance of verbal information is, at least in part, supported by the left pre-central gyrus, whereas scanning by the left inferior-frontal and supra-marginal gyri.SignificanceThe cortical structures involved in short-term maintenance and scanning of speech stimuli were segregated with an excellent temporal resolution.     

A Review of Effects of Spinal Cord Stimulation on Spectral Features in Resting-State Electroencephalography

BackgroundSpinal cord stimulation (SCS) is an effective therapy for patients with refractory chronic pain syndromes. Although studies have shown that SCS has both spinal and supraspinal effects, the current understanding of cortical effects is still limited. Neuroimaging techniques, such as magnetoencephalography (MEG) and electroencephalography (EEG), combined here as M/EEG, can reveal modulations in ongoing resting-state cortical activity. We aim to provide an overview of available literature on resting-state M/EEG in patients with chronic pain who have been treated with SCS.Materials and MethodsWe searched multiple online data bases for studies on SCS, chronic pain, and resting-state M/EEG. Primary outcome measures were changes in spectral features, combined with brain regions in which these changes occurred.ResultsWe included eight studies reporting various SCS paradigms (tonic, burst, high-dose, and high-frequency stimulation) and revealing heterogeneity in outcome parameters. We summarized changes in cortical activity in various frequency bands: theta (4–7 Hz), alpha (7–12 Hz), beta (13–30 Hz), and gamma (30–44 Hz). In multiple studies, the somatosensory cortex showed modulation of cortical activity under tonic, burst, and high-frequency stimulation. Changes in connectivity were found in the dorsal anterior cingulate cortex, dorsolateral prefrontal cortex, and parahippocampus.ConclusionsThe large heterogeneity observed in outcome measures is probably caused by the large variety in study designs, stimulation paradigms, and spectral features studied. Paresthesia-free paradigms have been compared with tonic stimulation in multiple studies. These studies suggest modulation of medial, lateral, and descending pathways for paresthesia-free stimulation, whereas tonic stimulation predominantly modulates lateral and descending pathways. Moreover, multiple studies have reported an increased alpha peak frequency, increased alpha power, and/or decreased theta power when SCS was compared with baseline, indicating modulation of thalamocortical pathways. Further studies with well-defined groups of responders and nonresponders to SCS are recommended to independently study the cortical effects of pain relief and SCS.     

Time course of gamma‐band oscillation associated with face processing in the inferior occipital gyrus and fusiform gyrus: A combined fMRI and MEG study

Debate continues over whether the inferior occipital gyrus (IOG) or the fusiform gyrus (FG) represents the first stage of face processing and what role these brain regions play. We investigated this issue by combining functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) in normal adults. Participants passively observed upright and inverted faces and houses. First, we identified the IOG and FG as face‐specific regions using fMRI. We applied beamforming source reconstruction and time–frequency analysis to MEG source signals to reveal the time course of gamma‐band activations in these regions. The results revealed that the right IOG showed higher gamma‐band activation in response to upright faces than to upright houses at 100 ms from the stimulus onset. Subsequently, the right FG showed greater gamma‐band response to upright faces versus upright houses at around 170 ms. The gamma‐band activation in the right IOG and right FG was larger in response to inverted faces than to upright faces at the later time window. These results suggest that (1) the gamma‐band activities occurs rapidly first in the IOG and next in the FG and (2) the gamma‐band activity in the right IOG at later time stages is involved in configuration processing for faces. Hum Brain Mapp 38:2067–2079, 2017. © 2017 Wiley Periodicals, Inc.     

Adaptive changes in the neuromagnetic response of the primary and association somatosensory areas following repetitive tactile hand stimulation in humans

Cortical adaptation in the primary somatosensory cortex (SI) has been probed using different stimulation modalities and recording techniques, in both human and animal studies. In contrast, considerably less knowledge has been gained about the adaptation profiles in other areas of the cortical somatosensory network. Using magnetoencephalography (MEG), we examined the patterns of short‐term adaptation for evoked responses in SI and somatosensory association areas during tactile stimulation applied to the glabrous skin of the hand. Cutaneous stimuli were delivered as trains of serial pulses with a constant frequency of 2 Hz and 4 Hz in separate runs, and a constant inter‐train interval of 5 s. The unilateral stimuli elicited transient responses to the serial pulses in the train, with several response components that were separated by independent component analysis. Subsequent source reconstruction techniques identified regional generators in the contralateral SI and somatosensory association areas in the posterior parietal cortex (PPC). Activity in the bilateral secondary somatosensory cortex (i.e., SII/PV) was also identified, although less consistently across subjects. The dynamics of the evoked activity in each area and the frequency‐dependent adaptation effects were assessed from the changes in the relative amplitude of serial responses in each train. We show that the adaptation profiles in SI and PPC areas can be quantitatively characterized from neuromagnetic recordings using tactile stimulation, with the sensitivity to repetitive stimulation increasing from SI to PPC. A similar approach for SII/PV has proven less straightforward, potentially due to the tendency of these areas to respond selectively to certain stimuli. Hum Brain Mapp, 2013. © 2012 Wiley Perodicals, Inc.     

Cognitive loading via mental arithmetic modulates effects of blink‐related oscillations on precuneus and ventral attention network regions

Blink‐related oscillations (BROs) have been linked with environmental monitoring processes associated with blinking, with cortical activations in the bilateral precuneus. Although BROs have been described under resting and passive fixation conditions, little is known about their characteristics under cognitive loading. To address this, we investigated BRO effects during both mental arithmetic (MA) and passive fixation (PF) tasks using magnetoencephalography (n =20), while maintaining the same sensory environment in both tasks. Our results confirmed the presence of BRO effects in both MA and PF tasks, with similar characteristics including blink‐related increase in global field power and blink‐related activation of the bilateral precuneus. In addition, cognitive loading due to MA also modulated BRO effects by decreasing BRO‐induced cortical activations in key brain regions including the bilateral anterior precuneus. Interestingly, blinking during MA—but not PF—activated regions of the ventral attention network (i.e., right supramarginal gyrus and inferior frontal gyrus), suggesting possible recruitment of these areas for blink processing under cognitive loading conditions. Time–frequency analysis revealed a consistent pattern of BRO‐related effects in the precuneus in both tasks, but with task‐related functional segregation within the anterior and posterior subregions. Based on these findings, we postulate a potential neurocognitive mechanism for blink processing in the precuneus. This study is the first investigation of BRO effects under cognitive loading, and our results provide compelling new evidence for the important cognitive implications of blink‐related processing in the human brain.     

The engagement of mid-ventrolateral prefrontal cortex and posterior brain regions in intentional cognitive activity

It is now widely recognized that cognitive processes are carried out by a distributed network of brain areas, some of which are involved in perceptual processing of a stimulus, whilst others are involved in cognitive control processes required to carry out certain tasks. In this study, differential contributions of higher visual areas and of an area involved in cognitive control processes were investigated in a task requiring participants to simply look at a stimulus or to look with the intention of remembering. Varying the extent to which intentional cognitive processes were required and the stimulus material in this task allowed the analysis of "top-down" and "bottom-up" influences on these areas, respectively. Significant increases in the mid-ventrolateral prefrontal cortex (mid-VLPFC) were only observed when the stimuli were viewed with an intention in mind, irrespective of the stimulus type. In contrast, activity in the parahippocampal place area and the fusiform face area, was only modulated in conditions requiring intentional control when stimuli were presented that also elicited activity in these regions during passive viewing. These findings help to clarify the complimentary role that the mid-VLPFC and posterior higher visual areas play in controlled and relatively automatic memory processing.     

Time course of superior temporal sulcus activity in response to eye gaze: a combined fMRI and MEG study

The human superior temporal sulcus (STS) has been suggested to be involved in gaze processing, but temporal data regarding this issue are lacking. We investigated this topic by combining fMRI and MEG in four normal subjects. Photographs of faces with either averted or straight eye gazes were presented and subjects passively viewed the stimuli. First, we analyzed the brain areas involved using fMRI. A group analysis revealed activation of the STS for averted compared to straight gazes, which was confirmed in all subjects. We then measured brain activity using MEG, and conducted a 3D spatial filter analysis. The STS showed higher activity in response to averted versus straight gazes during the 150–200 ms period, peaking at around 170 ms, after stimulus onset. In contrast, the fusiform gyrus, which was detected by the main effect of stimulus presentations in fMRI analysis, exhibited comparable activity across straight and averted gazes at about 170 ms. These results indicate involvement of the human STS in rapid processing of the eye gaze of another individual.     

Early dissociation of face and object processing: a magnetoencephalographic study

The early dissociation in cortical responses to faces and objects was explored with magnetoencephalographic (MEG) recordings and source localization. To control for differences in the low-level stimulus features, which are known to modulate early brain responses, we created a novel set of stimuli so that their combinations did not have any differences in the visual-field location, spatial frequency, or luminance contrast. Differing responses to face and object (flower) stimuli were found at about 100 ms after stimulus onset in the occipital cortex. Our data also confirm that the brain response to a complex visual stimulus is not merely a sum of the responses to its constituent parts; the nonlinearity in the response was largest for meaningful stimuli.     

Spindle–slow oscillation coupling correlates with memory performance and connectivity changes in a hippocampal network after sleep

After experiences are encoded, post‐encoding reactivations during sleep have been proposed to mediate long‐term memory consolidation. Spindle–slow oscillation coupling during NREM sleep is a candidate mechanism through which a hippocampal‐cortical dialogue may strengthen a newly formed memory engram. Here, we investigated the role of fast spindle‐ and slow spindle–slow oscillation coupling in the consolidation of spatial memory in humans with a virtual watermaze task involving allocentric and egocentric learning strategies. Furthermore, we analyzed how resting‐state functional connectivity evolved across learning, consolidation, and retrieval of this task using a data‐driven approach. Our results show task‐related connectivity changes in the executive control network, the default mode network, and the hippocampal network at post‐task rest. The hippocampal network could further be divided into two subnetworks of which only one showed modulation by sleep. Decreased functional connectivity in this subnetwork was associated with higher spindle–slow oscillation coupling power, which was also related to better memory performance at test. Overall, this study contributes to a more holistic understanding of the functional resting‐state networks and the mechanisms during sleep associated to spatial memory consolidation.