Modulation of alpha oscillations by attention is predicted by hemispheric asymmetry of subcortical regions.

Evidence suggests that subcortical structures play a role in high-level cognitive functions such as the allocation of spatial attention. While there is abundant evidence in humans for posterior alpha band oscillations being modulated by spatial attention, little is known about how subcortical regions contribute to these oscillatory modulations, particularly under varying conditions of cognitive challenge. In this study, we combined MEG and structural MRI data to investigate the role of subcortical structures in controlling the allocation of attentional resources by employing a cued spatial attention paradigm with varying levels of perceptual load. We asked whether hemispheric lateralization of volumetric measures of the thalamus and basal ganglia predicted the hemispheric modulation of alpha-band power. Lateral asymmetry of the globus pallidus, caudate nucleus, and thalamus predicted attention-related modulations of posterior alpha oscillations. When the perceptual load was applied to the target and the distractor was salient caudate nucleus asymmetry predicted alpha-band modulations. Globus pallidus was predictive of alpha-band modulations when either the target had a high load, or the distractor was salient, but not both. Finally, the asymmetry of the thalamus predicted alpha band modulation when neither component of the task was perceptually demanding. In addition to delivering new insight into the subcortical circuity controlling alpha oscillations with spatial attention, our finding might also have clinical applications. We provide a framework that could be followed for detecting how structural changes in subcortical regions that are associated with neurological disorders can be reflected in the modulation of oscillatory brain activity.

A New Generation of OPM for High Dynamic and Large Bandwidth MEG: The 4He OPMs-First Applications in Healthy Volunteers.

MagnetoEncephaloGraphy (MEG) provides a measure of electrical activity in the brain at a millisecond time scale. From these signals, one can non-invasively derive the dynamics of brain activity. Conventional MEG systems (SQUID-MEG) use very low temperatures to achieve the necessary sensitivity. This leads to severe experimental and economical limitations. A new generation of MEG sensors is emerging: the optically pumped magnetometers (OPM). In OPM, an atomic gas enclosed in a glass cell is traversed by a laser beam whose modulation depends on the local magnetic field. MAG4Health is developing OPMs using Helium gas (4He-OPM). They operate at room temperature with a large dynamic range and a large frequency bandwidth and output natively a 3D vectorial measure of the magnetic field. In this study, five 4He-OPMs were compared to a classical SQUID-MEG system in a group of 18 volunteers to evaluate their experimental performances. Considering that the 4He-OPMs operate at real room temperature and can be placed directly on the head, our assumption was that 4He-OPMs would provide a reliable recording of physiological magnetic brain activity. Indeed, the results showed that the 4He-OPMs showed very similar results to the classical SQUID-MEG system by taking advantage of a shorter distance to the brain, despite having a lower sensitivity.

Spatial Attention Tunes Temporal Processing in Early Visual Cortex by Speeding and Slowing Alpha Oscillations.

The perception of dynamic visual stimuli relies on two apparently conflicting perceptual mechanisms: rapid visual input must sometimes be integrated into unitary percepts but at other times must be segregated or parsed into separate objects or events. Though they have opposite effects on our perceptual experience, the deployment of spatial attention benefits both operations. Little is known about the neural mechanisms underlying this impact of spatial attention on temporal perception. Here, we record magnetoencephalography (MEG) in male and female humans to demonstrate that the deployment of spatial attention for the purpose of segregating or integrating visual stimuli impacts prestimulus oscillatory activity in retinotopic visual brain areas where the attended location is represented. Alpha band oscillations contralateral to an attended location are therefore faster than ipsilateral oscillations when stimuli appearing at this location will need to be segregated, but slower in expectation of the need for integration, consistent with the idea that α frequency is linked to perceptual sampling rate. These results demonstrate a novel interaction between temporal visual processing and the allocation of attention in space.SIGNIFICANCE STATEMENT Our environment is dynamic and visual input therefore varies over time. To make sense of continuously changing information, our visual system balances two complementary processes: temporal segregation in order to identify changes, and temporal integration to identify consistencies in time. When we know that a circumstance requires use of one or the other of these operations, we are able to prepare for this, and this preparation can be tracked in oscillatory brain activity. Here, we show how this preparation for temporal processing can be focused spatially. When we expect to integrate or segregate visual stimuli that will appear at a specific location, oscillatory brain activity changes in visual areas responsible for the representation of that location. In this way, spatial and temporal mechanisms interact to support adaptive, efficient perception.

Alpha oscillations reflect suppression of distractors with increased perceptual load.

Attention serves an essential role in cognition and behavior allowing us to focus on behaviorally-relevant objects while ignoring distraction. Perceptual load theory states that attentional resources are allocated according to the requirements of the task, i.e., its 'load'. The theory predicts that the resources left to process irrelevant, possibly distracting stimuli, are reduced when the perceptual load is high. However, it remains unclear how this allocation of attentional resources specifically relates to neural excitability and suppression mechanisms. In this magnetoencephalography (MEG) study, we show that brain oscillations in the alpha band (8-13 Hz) implemented the suppression of distracting objects when the perceptual load was high. In parallel, high load increased the neuronal excitability for target objects, as reflected by rapid invisible frequency tagging. We suggest that the allocation of resources in tasks with high perceptual load is implemented by a gain increase for targets, complemented by distractor suppression reflected by alpha-band oscillations closing the 'gate' for interference.

No Evidence for Entrainment: Endogenous Gamma Oscillations and Rhythmic Flicker Responses Coexist in Visual Cortex.

Over the past decades, numerous studies have linked cortical gamma oscillations (∼30-100 Hz) to neurocomputational mechanisms. Their functional relevance, however, is still passionately debated. Here, we asked whether endogenous gamma oscillations in the human brain can be entrained by a rhythmic photic drive >50 Hz. Such a noninvasive modulation of endogenous brain rhythms would allow conclusions about their causal involvement in neurocognition. To this end, we systematically investigated oscillatory responses to a rapid sinusoidal flicker in the absence and presence of endogenous gamma oscillations using magnetoencephalography (MEG) in combination with a high-frequency projector. The photic drive produced a robust response over visual cortex to stimulation frequencies of up to 80 Hz. Strong, endogenous gamma oscillations were induced using moving grating stimuli as repeatedly done in previous research. When superimposing the flicker and the gratings, there was no evidence for phase or frequency entrainment of the endogenous gamma oscillations by the photic drive. Unexpectedly, we did not observe an amplification of the flicker response around participants' individual gamma frequencies (IGFs); rather, the magnitude of the response decreased monotonically with increasing frequency. Source reconstruction suggests that the flicker response and the gamma oscillations were produced by separate, coexistent generators in visual cortex. The presented findings challenge the notion that cortical gamma oscillations can be entrained by rhythmic visual stimulation. Instead, the mechanism generating endogenous gamma oscillations seems to be resilient to external perturbation.SIGNIFICANCE STATEMENT We aimed to investigate to what extent ongoing, high-frequency oscillations in the gamma-band (30-100 Hz) in the human brain can be entrained by a visual flicker. Gamma oscillations have long been suggested to coordinate neuronal firing and enable interregional communication. Our results demonstrate that rhythmic visual stimulation cannot hijack the dynamics of ongoing gamma oscillations; rather, the flicker response and the endogenous gamma oscillations coexist in different visual areas. Therefore, while a visual flicker evokes a strong neuronal response even at high frequencies in the gamma-band, it does not entrain endogenous gamma oscillations in visual cortex. This has important implications for interpreting studies investigating the causal and neuroprotective effects of rhythmic sensory stimulation in the gamma-band.

Role of Alpha-Band Oscillations in Spatial Updating across Whole Body Motion.

When moving around in the world, we have to keep track of important locations in our surroundings. In this process, called spatial updating, we must estimate our body motion and correct representations of memorized spatial locations in accordance with this motion. While the behavioral characteristics of spatial updating across whole body motion have been studied in detail, its neural implementation lacks detailed study. Here we use electroencephalography (EEG) to distinguish various spectral components of this process. Subjects gazed at a central body-fixed point in otherwise complete darkness, while a target was briefly flashed, either left or right from this point. Subjects had to remember the location of this target as either moving along with the body or remaining fixed in the world while being translated sideways on a passive motion platform. After the motion, subjects had to indicate the remembered target location in the instructed reference frame using a mouse response. While the body motion, as detected by the vestibular system, should not affect the representation of body-fixed targets, it should interact with the representation of a world-centered target to update its location relative to the body. We show that the initial presentation of the visual target induced a reduction of alpha band power in contralateral parieto-occipital areas, which evolved to a sustained increase during the subsequent memory period. Motion of the body led to a reduction of alpha band power in central parietal areas extending to lateral parieto-temporal areas, irrespective of whether the targets had to be memorized relative to world or body. When updating a world-fixed target, its internal representation shifts hemispheres, only when subjects' behavioral responses suggested an update across the body midline. Our results suggest that parietal cortex is involved in both self-motion estimation and the selective application of this motion information to maintaining target locations as fixed in the world or fixed to the body.

Schematic memory components converge within angular gyrus during retrieval.

Mental schemas form associative knowledge structures that can promote the encoding and consolidation of new and related information. Schemas are facilitated by a distributed system that stores components separately, presumably in the form of inter-connected neocortical representations. During retrieval, these components need to be recombined into one representation, but where exactly such recombination takes place is unclear. Thus, we asked where different schema components are neuronally represented and converge during retrieval. Subjects acquired and retrieved two well-controlled, rule-based schema structures during fMRI on consecutive days. Schema retrieval was associated with midline, medial-temporal, and parietal processing. We identified the multi-voxel representations of different schema components, which converged within the angular gyrus during retrieval. Critically, convergence only happened after 24-hour-consolidation and during a transfer test where schema material was applied to novel but related trials. Therefore, the angular gyrus appears to recombine consolidated schema components into one memory representation.

The Müller-Lyer illusion affects visuomotor updating in the dorsal visual stream.

To guide our actions, the brain has developed mechanisms to code target locations in egocentric coordinates (i.e., with respect to the observer), and to update these when the observer moves. The latter mechanism, called visuomotor updating, is implemented in the dorsal visual stream of the brain. In contrast, the ventral visual stream is assumed to transform target locations into an allocentric reference frame that is highly sensitive to visual contextual illusions. Here, we tested the effect of the Müller-Lyer illusion on visuomotor updating in a double-step saccade task. Using the same paradigm in a 3T fMRI scanner, we investigated the effect of the illusion on the neural correlate of the updating process. Participants briefly viewed the Brentano version of the Müller-Lyer illusion with a target at its middle vertex, while fixating at one of the two endpoints of the illusion. Shortly after the disappearance of the stimulus, the eyes' fixation point moved to a position outside the illusion. After a delay, participants made a saccade to the remembered position of the target. The landing position of this saccade was systematically displaced in a manner congruent with the perceptual illusion, showing that visuomotor updating is affected by the illusion. fMRI results showed that the BOLD response in the occipito-parietal cortex (area V7) and the intraparietal sulcus related to planning of the saccade to the updated target was also modulated by the configuration of the illusion. This suggests that the dorsal visual stream represents perceived rather than physical locations of remembered saccade targets.

Action preparation shapes processing in early visual cortex.

Preparation for an action, such as grasping an object, is accompanied by an enhanced perception of the object's action-relevant features, such as orientation and size. Cortical feedback from motor planning areas to early visual areas may drive this enhanced perception. To examine whether action preparation modulates activity in early human visual cortex, subjects grasped or pointed to oriented objects while high-resolution fMRI data were acquired. Using multivoxel pattern analysis techniques, we could decode with >70% accuracy whether a grasping or pointing action was prepared from signals in visual cortex as early as V1. These signals in early visual cortex were observed even when actions were only prepared but not executed. Anterior parietal cortex, on the other hand, showed clearest modulation for actual movements. This demonstrates that preparation of actions, even without execution, modulates relevant neuronal populations in early visual areas.

Proactive control of sequential saccades in the human supplementary eye field.

Our ability to regulate behavior based on past experience has thus far been examined using single movements. However, natural behavior typically involves a sequence of movements. Here, we examined the effect of previous trial type on the concurrent planning of sequential saccades using a unique paradigm. The task consisted of two trial types: no-shift trials, which implicitly encouraged the concurrent preparation of the second saccade in a subsequent trial; and target-shift trials, which implicitly discouraged the same in the next trial. Using the intersaccadic interval as an index of concurrent planning, we found evidence for context-based preparation of sequential saccades. We also used functional MRI-guided, single-pulse, transcranial magnetic stimulation on human subjects to test the role of the supplementary eye field (SEF) in the proactive control of sequential eye movements. Results showed that (i) stimulating the SEF in the previous trial disrupted the previous trial type-based preparation of the second saccade in the nonstimulated current trial, (ii) stimulating the SEF in the current trial rectified the disruptive effect caused by stimulation in the previous trial, and (iii) stimulating the SEF facilitated the preparation of second saccades based on previous trial type even when the previous trial was not stimulated. Taken together, we show how the human SEF is causally involved in proactive preparation of sequential saccades.

A functional and structural investigation of the human fronto-basal volitional saccade network.

Almost all cortical areas are connected to the subcortical basal ganglia (BG) through parallel recurrent inhibitory and excitatory loops, exerting volitional control over automatic behavior. As this model is largely based on non-human primate research, we used high resolution functional MRI and diffusion tensor imaging (DTI) to investigate the functional and structural organization of the human (pre)frontal cortico-basal network controlling eye movements. Participants performed saccades in darkness, pro- and antisaccades and observed stimuli during fixation. We observed several bilateral functional subdivisions along the precentral sulcus around the human frontal eye fields (FEF): a medial and lateral zone activating for saccades in darkness, a more fronto-medial zone preferentially active for ipsilateral antisaccades, and a large anterior strip along the precentral sulcus activating for visual stimulus presentation during fixation. The supplementary eye fields (SEF) were identified along the medial wall containing all aforementioned functions. In the striatum, the BG area receiving almost all cortical input, all saccade related activation was observed in the putamen, previously considered a skeletomotor striatal subdivision. Activation elicited by the cue instructing pro or antisaccade trials was clearest in the medial FEF and right putamen. DTI fiber tracking revealed that the subdivisions of the human FEF complex are mainly connected to the putamen, in agreement with the fMRI findings. The present findings demonstrate that the human FEF has functional subdivisions somewhat comparable to non-human primates. However, the connections to and activation in the human striatum preferentially involve the putamen, not the caudate nucleus as is reported for monkeys. This could imply that fronto-striatal projections for the oculomotor system are fundamentally different between humans and monkeys. Alternatively, there could be a bias in published reports of monkey studies favoring the caudate nucleus over the putamen in the search for oculomotor functions.

Transcranial magnetic stimulation and motor plasticity in human lateral cerebellum: dual effect on saccadic adaptation.

The cerebellum is a key area for movement control and sensory-motor plasticity. Its medial part is considered as the exclusive cerebellar center controlling the accuracy and adaptive calibration of saccadic eye movements. However, the contribution of other zones situated in its lateral part is unknown. We addressed this question in healthy adult volunteers by using magnetic resonance imaging (MRI)-guided transcranial magnetic stimulation (TMS). The double-step target paradigm was used to adaptively lengthen or shorten saccades. TMS pulses over the right hemisphere of the cerebellum were delivered at 0, 30, or 60 ms after saccade detection in separate recording sessions. The effects on saccadic adaptation were assessed relative to a fourth session where TMS was applied to Vertex as a control site. First, TMS applied upon saccade detection before the adaptation phase reduced saccade accuracy. Second, TMS applied during the adaptation phase had a dual effect on saccadic plasticity: adaptation after-effects revealed a potentiation of the adaptive lengthening and a depression of the adaptive shortening of saccades. For the first time, we demonstrate that TMS on lateral cerebellum can influence plasticity mechanisms underlying motor performance. These findings also provide the first evidence that the human cerebellar hemispheres are involved in the control of saccade accuracy and in saccadic adaptation, with possibly different neuronal populations concerned in adaptive lengthening and shortening. Overall, these results require a reappraisal of current models of cerebellar contribution to oculomotor plasticity.

Grasping preparation enhances orientation change detection.

Preparing a goal directed movement often requires detailed analysis of our environment. When picking up an object, its orientation, size and relative distance are relevant parameters when preparing a successful grasp. It would therefore be beneficial if the motor system is able to influence early perception such that information processing needs for action control are met at the earliest possible stage. However, only a few studies reported (indirect) evidence for action-induced visual perception improvements. We therefore aimed to provide direct evidence for a feature-specific perceptual modulation during the planning phase of a grasping action. Human subjects were instructed to either grasp or point to a bar while simultaneously performing an orientation discrimination task. The bar could slightly change its orientation during grasping preparation. By analyzing discrimination response probabilities, we found increased perceptual sensitivity to orientation changes when subjects were instructed to grasp the bar, rather than point to it. As a control experiment, the same experiment was repeated using bar luminance changes, a feature that is not relevant for either grasping or pointing. Here, no differences in visual sensitivity between grasping and pointing were found. The present results constitute first direct evidence for increased perceptual sensitivity to a visual feature that is relevant for a certain skeletomotor act during the movement preparation phase. We speculate that such action-induced perception improvements are controlled by neuronal feedback mechanisms from cortical motor planning areas to early visual cortex, similar to what was recently established for spatial perception improvements shortly before eye movements.

Lateralized frontal eye field activity precedes occipital activity shortly before saccades: evidence for cortico-cortical feedback as a mechanism underlying covert attention shifts.

When an eye movement is prepared, attention is shifted toward the saccade end-goal. This coupling of eye movements and spatial attention is thought to be mediated by cortical connections between the FEFs and the visual cortex. Here, we present evidence for the existence of these connections. A visual discrimination task was performed while recording the EEG. Discrimination performance was significantly improved when the discrimination target and the saccade target matched. EEG results show that frontal activity precedes occipital activity contralateral to saccade direction when the saccade is prepared but not yet executed; these effects were absent in fixation conditions. This is consistent with the idea that the FEF exerts a direct modulatory influence on the visual cortex and enhances perception at the saccade end-goal.