Spontaneous blink-related beta power increase and theta phase reset in subthalamic nucleus of Parkinson patients during walking.

OBJECTIVE: Both blinking and walking are altered in Parkinson's disease and both motor outputs have been shown to be linked in healthy subjects. Additionally, studies suggest an involvement of basal ganglia activity and striatal dopamine in blink generation. We investigated the role of the basal ganglia circuitry on spontaneous blinking and if this role is dependent on movement state and striatal dopamine. METHODS: We analysed subthalamic nucleus (STN) activity in seven chronically implanted patients for deep brain stimulation (DBS) with respect to blinks and movement state (resting state and unperturbed walking). Neurophysiological recordings were combined with individual molecular brain imaging assessing the dopamine reuptake transporter (DAT) density for the left and right striatum separately. RESULTS: We found a significantly higher blink rate during walking compared to resting. The blink rate during walking positively correlated with the DAT density of the left caudate nucleus. During walking only, spontaneous blinking was followed by an increase in the right STN beta power and a bilateral subthalamic phase reset in the low frequencies. The right STN blink-related beta power modulation correlated negatively with the DAT density of the contralateral putamen. The left STN blink-related beta power correlated with the DAT density of the putamen in the less dopamine-depleted hemisphere. Both correlations were specific to the walking condition and to beta power following a blink. CONCLUSION: Our findings show that spontaneous blinking is related to striatal dopamine and has a frequency specific deployment in the STN. This correlation depends on the current movement state such as walking. SIGNIFICANCE: This work indicates that subcortical activity following a motor event as well as the relationship between dopamine and motor events can be dependent on the motor state. Accordingly, disease related changes in brain activity should be assessed during natural movement.

Spontaneous Eye Blinks Map the Probability of Perceptual Reinterpretation During Visual and Auditory Ambiguity.

Spontaneous eye blinks are modulated around perceptual events. Our previous study, using a visual ambiguous stimulus, indicated that blink probability decreases before a reported perceptual switch. In the current study, we tested our hypothesis that an absence of blinks marks a time in which perceptual switches are facilitated in- and outside the visual domain. In three experiments, presenting either a visual motion quartet in light or darkness or a bistable auditory streaming stimulus, we found a co-occurrence of blink rate reduction with increased perceptual switch probability. In the visual domain, perceptual switches induced by a short interruption of visual input (blank) allowed an estimate of the timing of the perceptual event with respect to the motor response. This provided the first evidence that the blink reduction was not a consequence of the perceptual switch. Importantly, by showing that the time between switches and the previous blink was significantly longer than the inter-blink interval, our studies allowed to conclude that perceptual switches did not happen at random but followed a prolonged period of nonblinking. Correspondingly, blink rate and switch rate showed an inverse relationship. Our study supports the idea that the absence or presence of blinks maps perceptual processes independent of the sensory modality.

Reduced occipital alpha power marks a movement induced state change that facilitates creative thinking.

Walking and minimized movement restriction has a positive effect on creativity, such as divergent thinking. Walking is further known to reduce occipital alpha activity. We used mobile EEG during free and restricted movement, while subjects (N = 23) solved a Guilford's alternate uses test, to understand if occipital alpha power is also affected by movement restriction and if it is a neural marker for creativity. We found that, independent of the task, relative occipital alpha power was higher during movement restriction and showed a negative relationship with creativity scores even though the task was purely based on auditory information. Alpha lateralization was only modulated during the task related think-time (mainly during sitting) and showed a positive relationship with creativity scores but no correlation with the relative alpha power. This indicates that the ongoing alpha power and alpha lateralization mark two independent processes. Overall, our work shows that movement and movement restriction leads to a general change in state which affects cognitive processes. Specifically, limiting one's movements e.g. due to sitting and fixating on a screen can introduce a state of increased occipital alpha power and lowered creativity.

Restoration of Attention by Rest in a Multitasking World: Theory, Methodology, and Empirical Evidence.

In this work, we evaluate the status of both theory and empirical evidence in the field of experimental rest-break research based on a framework that combines mental-chronometry and psychometric-measurement theory. To this end, we (1) provide a taxonomy of rest breaks according to which empirical studies can be classified (e.g., by differentiating between long, short, and micro-rest breaks based on context and temporal properties). Then, we (2) evaluate the theorizing in both the basic and applied fields of research and explain how popular concepts (e.g., ego depletion model, opportunity cost theory, attention restoration theory, action readiness, etc.) relate to each other in contemporary theoretical debates. Here, we highlight differences between all these models in the light of two symbolic categories, termed the resource-based and satiation-based model, including aspects related to the dynamics and the control (strategic or non-strategic) mechanisms at work. Based on a critical assessment of existing methodological and theoretical approaches, we finally (3) provide a set of guidelines for both theory building and future empirical approaches to the experimental study of rest breaks. We conclude that a psychometrically advanced and theoretically focused research of rest and recovery has the potential to finally provide a sound scientific basis to eventually mitigate the adverse effects of ever increasing task demands on performance and well-being in a multitasking world at work and leisure.

Motor restrictions impair divergent thinking during walking and during sitting.

Creativity, specifically divergent thinking, has been shown to benefit from unrestrained walking. Despite these findings, it is not clear if it is the lack of restriction that leads to the improvement. Our goal was to explore the effects of motor restrictions on divergent thinking for different movement states. In addition, we assessed whether spontaneous eye blinks, which are linked to motor execution, also predict performance. In experiment 1, we compared the performance in Guilford's alternate uses task (AUT) during walking vs. sitting, and analysed eye blink rates during both conditions. We found that AUT scores were higher during walking than sitting. Albeit eye blinks differed significantly between movement conditions (walking vs. sitting) and task phase (baseline vs. thinking vs. responding), they did not correlate with task performance. In experiment 2 and 3, participants either walked freely or in a restricted path, or sat freely or fixated on a screen. When the factor restriction was explicitly modulated, the effect of walking was reduced, while restriction showed a significant influence on the fluency scores. Importantly, we found a significant correlation between the rate of eye blinks and creativity scores between subjects, depending on the restriction condition. Our study shows a movement state-independent effect of restriction on divergent thinking. In other words, similar to unrestrained walking, unrestrained sitting also improves divergent thinking. Importantly, we discuss a mechanistic explanation of the effect of restriction on divergent thinking based on the increased size of the focus of attention and the consequent bias towards flexibility.

How the motor aspect of speaking influences the blink rate.

The blink rate increases if a person indulges in a conversation compared to quiet rest. Since various factors were suggested to explain this increase, the present series of studies tested the influence of different motor activities, cognitive processes and auditory input on the blink behavior but at the same time minimized visual stimulation as well as social influences. Our results suggest that neither cognitive demands without verbalization, nor isolated lip, jaw or tongue movements, nor auditory input during vocalization or listening influence our blinking behavior. In three experiments, we provide evidence that complex facial movements during unvoiced speaking are the driving factors that increase blinking. If the complexity of the motor output increased such as during the verbalization of speech, the blink rate rose even more. Similarly, complex facial movements without cognitive demands, such as sucking on a lollipop, increased the blink rate. Such purely motor-related influences on blinking advise caution particularly when using blink rates assessed during patient interviews as a neurological indicator.

The latency of spontaneous eye blinks marks relevant visual and auditory information processing.

Eye blinks are influenced by external sensory and internal cognitive factors, as mainly shown in the visual domain. In previous studies, these factors corresponded to the time period of task-relevant sensory information and were often linked to a motor response. Our aim was to dissociate the influence of overall sensory input duration, task-relevant information duration, and the motor response to further understand how the temporal modulation of blinks compares among sensory modalities. Using a visual and an auditory temporal judgment task, we found that blinks were suppressed during stimulus presentation in both domains and that the overall input length had a significant positive relationship with the length of this suppression (i.e., with the latency of the first blink after stimulus onset). Importantly, excluding the influence of the overall sensory input duration we could show that the duration of task-relevant input had an additional influence on blink latency in the visual and the auditory domain. Our findings further suggest that this influence was not based on sensory input but on top-down processes. We could exclude task difficulty and the timing of the motor response as driving factors in the blink modulation. Our results suggest a sensory domain-independent modulation of blink latencies, introduced by changes in the length of the task-relevant, attended period. Therefore, not only do blinks mark the timing of sensory input or the preparation of the motor output, but they can also act as precise indicators of periods of cognitive processing.

The Role of Blinks, Microsaccades and their Retinal Consequences in Bistable Motion Perception.

Eye-related movements such as blinks and microsaccades are modulated during bistable perceptual tasks. However, if they play an active role during internal perceptual switches is not known. We conducted two experiments involving an ambiguous plaid stimulus, wherein participants were asked to continuously report their percept, which could consist of either unidirectional coherent or bidirectional component movement. Our main results show that blinks and microsaccades did not facilitate perceptual switches. On the contrary, a reduction in eye movements preceded the perceptual switch. Blanks, on the other hand, thought to mimic the retinal consequences of a blink, consistently led to a switch. Through the timing of the blank-introduced perceptual change, we were able to estimate the delay between the internal switch and the response. This delay further allowed us to evaluate that the reduction in blink probability co-occurred with the internal perceptual switch. Additionally, our results indicate that distinct internal processes underlie the switch to coherent vs. component percept. Blanks exclusively facilitated a switch to the coherent percept, and only the switch to coherent percept was followed by an increase in blink rate. In a second study, we largely replicated the findings and included a microsaccade analysis. Microsaccades only showed a weak relation with perceptual switches, but their direction was correlated with the perceived motion direction. Nevertheless, our data suggests an interaction between microsaccades and blinks by showing that microsaccades were differently modulated around blinks compared with blanks. This study shows that a reduction in eye movements precedes internal perceptual switches indicating that the rate of blinks can set the stage for a reinterpretation of sensory input. While a perceptual switch based on changed sensory input usually leads to an increase in blink rate, such an increase was only present after the perceptual switch to coherent motion but absent after the switch to component percept. This provides evidence of different underlying mechanism or internal consequence of the two perceptual switches and suggests that blinks can uncover differences in internal percept-related processes that are not evident from the percept itself.

Effects of vocal demands on pupil dilation.

Pupil dilation is known to be affected by a variety of factors, including physical (e.g., light) and cognitive sources of influence (e.g., mental load due to working memory demands, stimulus/response competition etc.). In the present experiment, we tested the extent to which vocal demands (speaking) can affect pupil dilation. Based on corresponding preliminary evidence found in a reanalysis of an existing data set from our lab, we setup a new experiment that systematically investigated vocal response-related effects compared to mere jaw/lip movement and button press responses. Conditions changed on a trial-by-trial basis while participants were instructed to keep fixating a central cross on a screen throughout. In line with our prediction (and previous observation), speaking caused the pupils to dilate strongest, followed by nonvocal movements and finally a baseline condition without any vocal or muscular demands. An additional analysis of blink rates showed no difference in blink frequency between vocal and baseline conditions, but different blink dynamics. Finally, simultaneously recorded electromyographic activity showed that muscle activity may contribute to some (but not all) aspects of the observed effects on pupil size. The results are discussed in the context of other recent research indicating effects of perceived (instead of executed) vocal action on pupil dynamics.

Disentangling top-down and bottom-up influences on blinks in the visual and auditory domain.

Sensory input as well as cognitive factors can drive the modulation of blinking. Our aim was to dissociate sensory driven bottom-up from cognitive top-down influences on blinking behavior and compare these influences between the auditory and the visual domain. Using an oddball paradigm, we found a significant pre-stimulus decrease in blink probability for visual input compared to auditory input. Sensory input further led to an early post-stimulus blink increase in both modalities if a task demanded attention to the input. Only visual input caused a pronounced early increase without a task. In case of a target or the omission of a stimulus (as compared to standard input), an additional late increase in blink rate was found in the auditory and visual domain. This suggests that blink modulation must be based on the interpretation of the input, but does not need any sensory input at all to occur. Our results show a complex modulation of blinking based on top-down factors such as prediction and attention in addition to sensory-based influences. The magnitude of the modulation is mainly influenced by general attentional demands, while the latency of this modulation allows dissociating general from specific top-down influences that are independent of the sensory domain.

Walking enhances peripheral visual processing in humans.

Cognitive processes are almost exclusively investigated under highly controlled settings during which voluntary body movements are suppressed. However, recent animal work suggests differences in sensory processing between movement states by showing drastically changed neural responses in early visual areas between locomotion and stillness. Does locomotion also modulate visual cortical activity in humans, and what are the perceptual consequences? Our study shows that walking increased the contrast-dependent influence of peripheral visual input on central visual input. This increase is prevalent in stimulus-locked electroencephalogram (EEG) responses (steady-state visual evoked potential [SSVEP]) alongside perceptual performance. Ongoing alpha oscillations (approximately 10 Hz) further positively correlated with the walking-induced changes of SSVEP amplitude, indicating the involvement of an altered inhibitory process during walking. The results predicted that walking leads to an increased processing of peripheral visual input. A second study indeed showed an increased contrast sensitivity for peripheral compared to central stimuli when subjects were walking. Our work shows complementary neurophysiological and behavioural evidence corroborating animal findings that walking leads to a change in early visual neuronal activity in humans. That neuronal modulation due to walking is indeed linked to specific perceptual changes extends the existing animal work.

Spontaneous local alpha oscillations predict motion-induced blindness.

Bistable visual illusions are well suited for exploring the neuronal states of the brain underlying changes in perception. In this study, we investigated oscillatory activity associated with 'motion-induced blindness' (MIB), which denotes the perceptual disappearance of salient target stimuli when a moving pattern is superimposed on them (Bonneh et al., ). We applied an MIB paradigm in which illusory target disappearances would occur independently in the left and right hemifields. Both illusory and real target disappearance were followed by an alpha lateralization with weaker contralateral than ipsilateral alpha activity (~10 Hz). However, only the illusion showed early alpha lateralization in the opposite direction, which preceded the alpha effect present for both conditions and coincided with the estimated onset of the illusion. The duration of the illusory disappearance was further predicted by the magnitude of this early lateralization when considered over subjects. In the gamma band (60-80 Hz), we found an increase in activity contralateral relative to ipsilateral only after a real disappearance. Whereas early alpha activity was predictive of onset and length of the illusory percept, gamma activity showed no modulation in relation to the illusion. Our study demonstrates that the spontaneous changes in visual alpha activity have perceptual consequences.

Cortical representations of confidence in a visual perceptual decision.

To date the exact neuronal implementation of decision confidence has been subject to little research. Here we explore electroencephalographic correlates of human choice certainty in a visual motion discrimination task for either spatial attention or motor effector cue instructions. We demonstrate electrophysiological correlates of choice certainty that evolve as early as 300 ms after stimulus onset and resemble the primary visual motion representations in early visual cortex. These correlates do not emerge unless or until the subject unambiguously knows which of the competing visual stimuli is actually relevant to behaviour. They extend beyond stimulus presentation up to the motor response but are independent of the motor effector. Our findings suggest that perceptual confidence evolves in parallel with representations of stimulus properties and is dedicated to one specific aspect of the visual world. Its electroencephalographic correlates can be disentangled from representations of sensory evidence, objective discrimination performance and overt motor behaviour.

Real color captures attention and overrides spatial cues in grapheme-color synesthetes but not in controls.

Grapheme-color synesthetes perceive color when reading letters or digits. We investigated oscillatory brain signals of synesthetes vs. controls using magnetoencephalography. Brain oscillations specifically in the alpha band (∼10Hz) have two interesting features: alpha has been linked to inhibitory processes and can act as a marker for attention. The possible role of reduced inhibition as an underlying cause of synesthesia, as well as the precise role of attention in synesthesia is widely discussed. To assess alpha power effects due to synesthesia, synesthetes as well as matched controls viewed synesthesia-inducing graphemes, colored control graphemes, and non-colored control graphemes while brain activity was recorded. Subjects had to report a color change at the end of each trial which allowed us to assess the strength of synesthesia in each synesthete. Since color (synesthetic or real) might allocate attention we also included an attentional cue in our paradigm which could direct covert attention. In controls the attentional cue always caused a lateralization of alpha power with a contralateral decrease and ipsilateral alpha increase over occipital sensors. In synesthetes, however, the influence of the cue was overruled by color: independent of the attentional cue, alpha power decreased contralateral to the color (synesthetic or real). This indicates that in synesthetes color guides attention. This was confirmed by reaction time effects due to color, i.e. faster RTs for the color side independent of the cue. Finally, the stronger the observed color dependent alpha lateralization, the stronger was the manifestation of synesthesia as measured by congruency effects of synesthetic colors on RTs. Behavioral and imaging results indicate that color induces a location-specific, automatic shift of attention towards color in synesthetes but not in controls. We hypothesize that this mechanism can facilitate coupling of grapheme and color during the development of synesthesia.

Top-down controlled alpha band activity in somatosensory areas determines behavioral performance in a discrimination task.

The brain receives a rich flow of information which must be processed according to behavioral relevance. How is the state of the sensory system adjusted to up- or downregulate processing according to anticipation? We used magnetoencephalography to investigate whether prestimulus alpha band activity (8-14 Hz) reflects allocation of attentional resources in the human somatosensory system. Subjects performed a tactile discrimination task where a visual cue directed attention to their right or left hand. The strength of attentional modulation was controlled by varying the reliability of the cue in three experimental blocks (100%, 75%, or 50% valid cueing). While somatosensory prestimulus alpha power lateralized strongly with a fully predictive cue (100%), lateralization was decreased with lower cue reliability (75%) and virtually absent if the cue had no predictive value at all (50%). Importantly, alpha lateralization influenced the subjects' behavioral performance positively: both accuracy and speed of response improved with the degree of alpha lateralization. This study demonstrates that prestimulus alpha lateralization in the somatosensory system behaves similarly to posterior alpha activity observed in visual attention tasks. Our findings extend the notion that alpha band activity is involved in shaping the functional architecture of the working brain by determining both the engagement and disengagement of specific regions: the degree of anticipation modulates the alpha activity in sensory regions in a graded manner. Thus, the alpha activity is under top-down control and seems to play an important role for setting the state of sensory regions to optimize processing.

Alpha oscillations correlate with the successful inhibition of unattended stimuli.

Because the human visual system is continually being bombarded with inputs, it is necessary to have effective mechanisms for filtering out irrelevant information. This is partly achieved by the allocation of attention, allowing the visual system to process relevant input while blocking out irrelevant input. What is the physiological substrate of attentional allocation? It has been proposed that alpha activity reflects functional inhibition. Here we asked if inhibition by alpha oscillations has behavioral consequences for suppressing the perception of unattended input. To this end, we investigated the influence of alpha activity on motion processing in two attentional conditions using magneto-encephalography. The visual stimuli used consisted of two random-dot kinematograms presented simultaneously to the left and right visual hemifields. Subjects were cued to covertly attend the left or right kinematogram. After 1.5 sec, a second cue tested whether subjects could report the direction of coherent motion in the attended (80%) or unattended hemifield (20%). Occipital alpha power was higher contralateral to the unattended side than to the attended side, thus suggesting inhibition of the unattended hemifield. Our key finding is that this alpha lateralization in the 20% invalidly cued trials did correlate with the perception of motion direction: Subjects with pronounced alpha lateralization were worse at detecting motion direction in the unattended hemifield. In contrast, lateralization did not correlate with visual discrimination in the attended visual hemifield. Our findings emphasize the suppressive nature of alpha oscillations and suggest that processing of inputs outside the field of attention is weakened by means of increased alpha activity.

Visual motion perception deficits due to cerebellar lesions are paralleled by specific changes in cerebro-cortical activity.

Recent anatomical studies have revealed strong cerebellar projections into parietal and prefrontal cortex. These findings suggest that the cerebellum might not only play a functional role in motor control but also cognitive domains, an idea also supported by neuropsychological testing of patients with cerebellar lesions that has revealed specific deficits. The goal of the present study was to test whether or not cognitive impairments after cerebellar damage are resulting from changes in cerebro-cortical signal processing. The detection of global visual motion embedded in noise, a faculty compromised after cerebellar lesions, was chosen as a model system. Using magnetoencephalography, cortical responses were recorded in a group of patients with cerebellar lesions (n = 8) and controls (n = 13) who observed visual motion of varied coherence, i.e., motion strength, presented in the peripheral visual field during controlled stationary fixation. Corroborating earlier results, the patients showed a significant impairment in global motion discrimination despite normal fixation behavior. This deficit was paralleled by qualitative differences in responses recorded from parieto-temporal cortex, including a reduced responsiveness to coherent visual motion and a striking loss of bilateral representations of motion coherence. Moreover, the perceptual thresholds correlated with the cortical representation of motion strength on single subject basis. These results demonstrate that visual motion processing in cerebral cortex critically depends on an intact cerebellum and establish a correlation between cortical activity and impaired visual perception resulting from cerebellar damage.

Cross-frequency coupling of brain oscillations indicates the success in visual motion discrimination.

Cortical activity such as recorded by EEG or MEG is characterized by ongoing rhythms that encompass a wide range of temporal and spatial scales. Recent studies have suggested an oscillatory hierarchy with faster oscillations being locked to preferred phases of underlying slower waves, a functional principle applied up to the level of action potential generation. We here tested the idea that amplitude-phase coupling between frequencies might serve the detection of weak sensory signals. To this end we recorded neuromagnetic responses during a motion discrimination task using near-threshold stimuli. Amplitude modulation of occipital high-frequency oscillations in the gamma range (63+/-5 Hz) was phase locked to a slow-frequency oscillation in the delta band (1-5 Hz). Most importantly, the strength of gamma amplitude modulation reflected the success in visual discrimination. This correlation provides evidence for the hypothesis that coupling between low- and high-frequency brain oscillations subserves signal detection.

Selective attention increases the dependency of cortical responses on visual motion coherence in man.

Attention improves visual discrimination and consequently allows to discern stimuli with low signal-to-noise ratios that otherwise would remain undetected. We used magnetoencephalography (MEG) to test whether neuromagnetic responses recorded from occipito-temporal cortex, reflecting the size of visual motion signals embedded in noise (motion coherence), would mirror the perceptual changes induced by attention. Attention directed to a given hemifield increased and decreased the coherence modulation of the MEG response over contralateral and ipsilateral visual cortex, respectively, indicating a change in the neuronal signal-to-noise ratio at the population level.

Gamma oscillations underlying the visual motion aftereffect.

After having been exposed to strong visual motion in one direction, a subsequently presented stationary visual scene seems to move in the opposite direction. This motion aftereffect (MAE) is usually ascribed to short-term functional changes in cortical areas involved in visual motion analysis akin to adaptation. Using magnetoencephalography (MEG), we show increased global field activity due to the MAE which could mostly be explained by a dipole located near the putative location of human area MT+. We further demonstrate that the induced MAE is accompanied by a significant increase in gamma-band activity (GBA) recorded from parietooccipital cortex contralateral to the visual motion stimulus. This gamma oscillation most likely reflects an increase in neuronal response coherence due to decreased inhibition of a group of neurons with similar preferred direction, namely the direction opposite to the adapted one. A second focal GBA response was picked up by the most posterior sensors ipsilateral to the side of the stimulus, reflecting the size of the MAE, whose source could not be reliably located.