NREM sleep brain networks modulate cognitive recovery from sleep deprivation.

Decrease in cognitive performance after sleep deprivation followed by recovery after sleep suggests its key role, and especially non-rapid eye movement (NREM) sleep, in the maintenance of cognition. It remains unknown whether brain network reorganization in NREM sleep stages N2 and N3 can uniquely be mapped onto individual differences in cognitive performance after a recovery nap following sleep deprivation. Using resting state functional magnetic resonance imaging (fMRI), we quantified the integration and segregation of brain networks during NREM sleep stages N2 and N3 while participants took a 1-hour nap following 24-hour sleep deprivation, compared to well-rested wakefulness. Here, we advance a new analytic framework called the hierarchical segregation index (HSI) to quantify network segregation across spatial scales, from whole-brain to the voxel level, by identifying spatio-temporally overlapping large-scale networks and the corresponding voxel-to-region hierarchy. Our results show that network segregation increased in the default mode, dorsal attention and somatomotor networks during NREM sleep compared to wakefulness. Segregation within the visual, limbic, and executive control networks exhibited N2 versus N3 sleep-specific voxel-level patterns. More segregation during N3 was associated with worse recovery of working memory, executive attention, and psychomotor vigilance after the nap. The level of spatial resolution of network segregation varied among brain regions and was associated with the recovery of performance in distinct cognitive tasks. We demonstrated the sensitivity and reliability of voxel-level HSI to provide key insights into within-region variation, suggesting a mechanistic understanding of how NREM sleep replenishes cognition after sleep deprivation.

Sleep, learning, and memory in human research using noninvasive neuroimaging techniques.

An accumulating body of evidence indicates that sleep is beneficial for learning and memory. Task performance improves significantly after a period that includes sleep, whereas a lack of sleep nullifies or impairs such improvements. Our current knowledge about sleep's role in learning and memory has been obtained based on studies that were conducted in both animal models and human subjects. Nevertheless, how sleep promotes learning and memory in humans is not fully understood. In this review, we overview our current understating of how sleep may contribute to learning and memory, covering different roles of non-rapid eye movement and rapid eye movement sleep. We then discuss cutting-edge advanced techniques that are currently available, including simultaneous functional magnetic resonance imaging (fMRI) and electroencephalogram (EEG) and simultaneous functional magnetic resonance spectroscopy (fMRS) and EEG measurements, and evaluate how these may contribute to advance the understanding of the role of sleep in human cognition. We also highlight the current limitations and challenges using these methods and discuss ways that may allow us to overcome these limitations.

An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation.

Sleep deprivation (SD) leads to impairments in cognitive function. Here, we tested the hypothesis that cognitive changes in the sleep-deprived brain can be explained by information processing within and between large-scale cortical networks. We acquired functional magnetic resonance imaging (fMRI) scans of 20 healthy volunteers during attention and executive tasks following a regular night of sleep, a night of SD, and a recovery nap containing nonrapid eye movement (NREM) sleep. Overall, SD was associated with increased cortex-wide functional integration, driven by a rise of integration within cortical networks. The ratio of within versus between network integration in the cortex increased further in the recovery nap, suggesting that prolonged wakefulness drives the cortex towards a state resembling sleep. This balance of integration and segregation in the sleep-deprived state was tightly associated with deficits in cognitive performance. This was a distinct and better marker of cognitive impairment than conventional indicators of homeostatic sleep pressure, as well as the pronounced thalamocortical connectivity changes that occurs towards falling asleep. Importantly, restoration of the balance between segregation and integration of cortical activity was also related to performance recovery after the nap, demonstrating a bidirectional effect. These results demonstrate that intra- and interindividual differences in cortical network integration and segregation during task performance may play a critical role in vulnerability to cognitive impairment in the sleep-deprived state.

Evaluation of a personalized functional near infra-red optical tomography workflow using maximum entropy on the mean.

In the present study, we proposed and evaluated a workflow of personalized near infra-red optical tomography (NIROT) using functional near-infrared spectroscopy (fNIRS) for spatiotemporal imaging of cortical hemodynamic fluctuations. The proposed workflow from fNIRS data acquisition to local 3D reconstruction consists of: (a) the personalized optimal montage maximizing fNIRS channel sensitivity to a predefined targeted brain region; (b) the optimized fNIRS data acquisition involving installation of optodes and digitalization of their positions using a neuronavigation system; and (c) the 3D local reconstruction using maximum entropy on the mean (MEM) to accurately estimate the location and spatial extent of fNIRS hemodynamic fluctuations along the cortical surface. The workflow was evaluated on finger-tapping fNIRS data acquired from 10 healthy subjects for whom we estimated the reconstructed NIROT spatiotemporal images and compared with functional magnetic resonance imaging (fMRI) results from the same individuals. Using the fMRI activation maps as our reference, we quantitatively compared the performance of two NIROT approaches, the MEM framework and the conventional minimum norm estimation (MNE) method. Quantitative comparisons were performed at both single subject and group-level. Overall, our results suggested that MEM provided better spatial accuracy than MNE, while both methods offered similar temporal accuracy when reconstructing oxygenated (HbO) and deoxygenated hemoglobin (HbR) concentration changes evoked by finger-tapping. Our proposed complete workflow was made available in the brainstorm fNIRS processing plugin-NIRSTORM, thus providing the opportunity for other researchers to further apply it to other tasks and on larger populations.

Data-driven beamforming technique to attenuate ballistocardiogram artefacts in electroencephalography-functional magnetic resonance imaging without detecting cardiac pulses in electrocardiography recordings.

Simultaneous recording of electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) is a very promising non-invasive neuroimaging technique. However, EEG data obtained from the simultaneous EEG-fMRI are strongly influenced by MRI-related artefacts, namely gradient artefacts (GA) and ballistocardiogram (BCG) artefacts. When compared to the GA correction, the BCG correction is more challenging to remove due to its inherent variabilities and dynamic changes over time. The standard BCG correction (i.e., average artefact subtraction [AAS]), require detecting cardiac pulses from simultaneous electrocardiography (ECG) recording. However, ECG signals are also distorted and will become problematic for detecting reliable cardiac peaks. In this study, we focused on a beamforming spatial filtering technique to attenuate all unwanted source activities outside of the brain. Specifically, we applied the beamforming technique to attenuate the BCG artefact in EEG-fMRI, and also to recover meaningful task-based neural signals during an attentional network task (ANT) which required participants to identify visual cues and respond accurately. We analysed EEG-fMRI data in 20 healthy participants during the ANT, and compared four different BCG corrections (non-BCG corrected, AAS BCG corrected, beamforming + AAS BCG corrected, beamforming BCG corrected). We demonstrated that the beamforming approach did not only significantly reduce the BCG artefacts, but also significantly recovered the expected task-based brain activity when compared to the standard AAS correction. This data-driven beamforming technique appears promising especially for longer data acquisition of sleep and resting EEG-fMRI. Our findings extend previous work regarding the recovery of meaningful EEG signals by an optimized suppression of MRI-related artefacts.

Identifying Cortical Substrates Underlying the Phenomenology of Stereopsis and Realness: A Pilot fMRI Study.

Viewing a real scene or a stereoscopic image (e.g., 3D movies) with both eyes yields a vivid subjective impression of object solidity, tangibility, immersive negative space and sense of realness; something that is not experienced when viewing single pictures of 3D scenes normally with both eyes. This phenomenology, sometimes referred to as stereopsis, is conventionally ascribed to the derivation of depth from the differences in the two eye's images (binocular disparity). Here we report on a pilot study designed to explore if dissociable neural activity associated with the phenomenology of realness can be localized in the cortex. In order to dissociate subjective impression from disparity processing, we capitalized on the finding that the impression of realness associated with stereoscopic viewing can also be generated when viewing a single picture of a 3D scene with one eye through an aperture. Under a blocked fMRI design, subjects viewed intact and scrambled images of natural 3-D objects, and scenes under three viewing conditions: (1) single pictures viewed normally with both eyes (binocular); (2) single pictures viewed with one eye through an aperture (monocular-aperture); and (3) stereoscopic anaglyph images of the same scenes viewed with both eyes (binocular stereopsis). Fixed-effects GLM contrasts aimed at isolating the phenomenology of stereopsis demonstrated a selective recruitment of similar posterior parietal regions for both monocular and binocular stereopsis conditions. Our findings provide preliminary evidence that the cortical processing underlying the subjective impression of realness may be dissociable and distinct from the derivation of depth from disparity.

Dissociating neural activity associated with the subjective phenomenology of monocular stereopsis: An EEG study.

The subjective phenomenology associated with stereopsis, of solid tangible objects separated by a palpable negative space, is conventionally thought to be a by-product of the derivation of depth from binocular disparity. However, the same qualitative impression has been reported in the absence of disparity, e.g., when viewing pictorial images monocularly through an aperture. Here we aimed to explore if we could identify dissociable neural activity associated with the qualitative impression of stereopsis in the absence of the processing of binocular disparities. We measured EEG activity while subjects viewed pictorial (non-stereoscopic) images of 2D and 3D geometric forms under four different viewing conditions (binocular, monocular, binocular aperture, monocular aperture). EEG activity was analysed by oscillatory source localization (beamformer technique) to examine power change in occipital and parietal regions across viewing and stimulus conditions in targeted frequency bands (alpha: 8-13 Hz & gamma: 60-90 Hz). We observed expected event-related gamma synchronization and alpha desynchronization in occipital cortex and predominant gamma synchronization in parietal cortex across viewing and stimulus conditions. However, only the viewing condition predicted to generate the strongest impression of stereopsis (monocular aperture) revealed significantly elevated gamma synchronization within the parietal cortex for the critical contrasts (3D vs. 2D form). These findings suggest dissociable neural processes specific to the qualitative impression of stereopsis as distinguished from disparity processing.

Stroboscopic Vision When Interacting With Multiple Moving Objects: Perturbation Is Not the Same as Elimination.

Motivated by recent findings of improved perceptual processing and perceptual-motor skill following stroboscopic vision training, the current study examined the performance and acquisition effects of stroboscopic vision methods that afford a different visual experience. In Experiment 1, we conducted a within-subject design study to examine performance of a multiple object tracking (MOT) task in different stroboscopic vision conditions (Nike Vapor Strobe®, PLATO visual occlusion, and intermittent display presentation) operating at 5.6, 3.2, or 1.8 Hz. We found that participants maintained MOT performance in the Vapor Strobe condition irrespective of strobe rate. However, MOT performance deteriorated as strobe rate was reduced in the other two stroboscopic vision conditions. Moreover, at the lowest strobe rate (1.8 Hz) there was an increase in probe reaction time, thus indicating an increased attentional demand due to the stroboscopic vision. In Experiment 2, we conducted a mixed design study to examine if practice in different stroboscopic vision conditions (Nike Vapor Strobe® and PLATO visual occlusion) influenced acquisition of a novel precision-aiming task [i.e., multiple object avoidance (MOA) task] compared to a normal vision group. Participants in the PLATO visual occlusion group exhibited worse performance during practice than the Vapor Strobe and normal vision groups. At post-test, the Vapor Strobe group demonstrated greater success and reduced end-point error than the normal vision and PLATO groups. We interpret these findings as showing that both an intermittent perturbation (Nike Vapor Strobe®) and elimination (PLATO visual occlusion and intermittent display presentation) of visual motion and form are more attention demanding (Experiment 1), however, the intermittent perturbation, but not elimination, of visual motion and form can facilitate acquisition of perceptual-motor skill (Experiment 2) in situations where it is necessary to maintain and update a spatio-temporal representation of multiple moving objects.

Asymmetrical time-to-contact error with two moving objects persists across different vertical separations.

When human observers estimate the time-to-contact (TTC) of more than one object there is an asymmetric pattern of error consistent with prioritizing the lead object at the expense of the trail object. Here, we examined TTC estimation in a prediction motion task where two objects moved along horizontal trajectories (5 or 7.5 °/s) that had different vertical separation, and thus placed specific demands on visuospatial attention. Results showed that participants were able to accurately judge arrival order, irrespective of vertical separation, in all but two conditions where the object trajectories crossed close to the arrival location. Constant error was significantly higher for the object that trailed, as opposed to led, by 250 or 500 ms. Asymmetry in constant error between the lead and trail object was not influenced by vertical separation, and was also evident across a range of arrival times. However, while the lag between the two consecutive TTC estimations was scaled to the actual difference in object arrival times, lag did increase with vertical separation. Taken together, our results confirm that TTC estimation of two moving objects in the prediction motion task suffers from an asymmetrical interference, which is likely related to factors that influence attentional allocation.

Exploring the advantages of multiband fMRI with simultaneous EEG to investigate coupling between gamma frequency neural activity and the BOLD response in humans.

We established an optimal combination of EEG recording during sparse multiband (MB) fMRI that preserves high-resolution, whole-brain fMRI coverage while enabling broad-band EEG recordings which are uncorrupted by MRI gradient artefacts (GAs). We first determined the safety of simultaneous EEG recording during MB fMRI. Application of MB factor = 4 produced <1°C peak heating of electrode/hardware during 20 min of GE-EPI data acquisition. However, higher SAR sequences require specific safety testing, with greater heating observed using PCASL with MB factor = 4. Heating was greatest in the electrocardiogram channel, likely due to it possessing longest lead length. We investigated the effect of MB factor on the temporal signal-to-noise ratio for a range of GE-EPI sequences (varying MB factor and temporal interval between slice acquisitions). We found that, for our experimental purpose, the optimal acquisition was achieved with MB factor = 3, 3mm isotropic voxels, and 33 slices providing whole head coverage. This sequence afforded a 2.25 s duration quiet period (without GAs) in every 3 s TR. Using this sequence, we demonstrated the ability to record gamma frequency (55-80 Hz) EEG oscillations, in response to right index finger abduction, that are usually obscured by GAs during continuous fMRI data acquisition. In this novel application of EEG-MB fMRI to a motor task, we observed a positive correlation between gamma and BOLD responses in bilateral motor regions. These findings support and extend previous work regarding coupling between neural and hemodynamic measures of brain activity in humans and showcase the utility of EEG-MB fMRI for future investigations.

Stroboscopic vision and sustained attention during coincidence-anticipation.

We compared coincidence-anticipation performance in normal vision and stroboscopic vision as a function of time-on-task. Participants estimated the arrival time of a real object that moved with constant acceleration (-0.7, 0, +0.7 m/s2) in a pseudo-randomised order across 4 blocks of 30 trials in both vision conditions, received in a counter-balanced order. Participants (n = 20) became more errorful (accuracy and variability) in the normal vision condition as a function of time-on-task, whereas performance was maintained in the stroboscopic vision condition. We interpret these data as showing that participants failed to maintain coincidence-anticipation performance in the normal vision condition due to monotony and attentional underload. In contrast, the stroboscopic vision condition placed a greater demand on visual-spatial memory for motion extrapolation, and thus participants did not experience the typical vigilance decrement in performance. While short-term adaptation effects from practicing in stroboscopic vision are promising, future work needs to consider for how long participants can maintain effortful processing, and whether there are negative carry-over effects from cognitive fatigue when transferring to normal vision.

Motor contagion: the contribution of trajectory and end-points.

Increased involuntary arm movement deviation when observing an incongruent human arm movement has been interpreted as a strong indicator of motor contagion. Here, we examined the contribution of trajectory and end-point information on motor contagion by altering congruence between the stimulus and arm movement. Participants performed cyclical horizontal arm movements whilst simultaneously observing a stimulus representing human arm movement. The stimuli comprised congruent horizontal movements or vertical movements featuring incongruent trajectory and end-points. A novel, third, stimulus comprised curvilinear movements featuring congruent end-points, but an incongruent trajectory. In Experiment 1, our dependent variables indicated increased motor contagion when observing the vertical compared to horizontal movement stimulus. There was even greater motor contagion in the curvilinear stimulus condition indicating an additive effect of an incongruent trajectory comprising congruent end-points. In Experiment 2, this additive effect was also present when facing perpendicular to the display, and thus with end-points represented as a product of the movement rather than an external spatial reference. Together, these findings support the theory of event coding (Hommel et al., Behav Brain Sci 24:849-878, 2001), and the prediction that increased motor contagion takes place when observed and executed actions share common features (i.e., movement end-points).