Shlomit Yuval-Greenberg

Saccadic spike potentials in gamma-band EEG: characterization, detection and suppression.

Analysis of high-frequency (gamma-band) neural activity by means of non-invasive EEG is gaining increasing interest. However, we have recently shown that a saccade-related spike potential (SP) seriously confounds the analysis of EEG induced gamma-band responses (iGBR), as the SP eludes traditional EEG artifact rejection methods. Here we provide a comprehensive profile of the SP and evaluate methods for its detection and suppression, aiming to unveil true cerebral gamma-band activity. The SP appears consistently as a sharp biphasic deflection of about 22 ms starting at the saccade onset, with a frequency band of approximately 20-90 Hz. On the average, larger saccades elicit higher SP amplitudes. The SP amplitude gradually changes from the extra-ocular channels towards posterior sites with the steepest gradients around the eyes, indicating its ocular source. Although the amplitude and the sign of the SP depend on the choice of reference channel, the potential gradients remain the same and non-zero for all references. The scalp topography is modulated almost exclusively by the direction of saccades, with steeper gradients ipsilateral to the saccade target. We discuss how the above characteristics impede attempts to remove these SPs from the EEG by common temporal filtering, choice of different references, or rejection of contaminated trials. We examine the extent to which SPs can be reliably detected without an eye tracker, assess the degree to which scalp current density derivation attenuates the effect of the SP, and propose a tailored ICA procedure for minimizing the effect of the SP.

What You See Is Not (Always) What You Hear: Induced Gamma Band Responses Reflect Cross-Modal Interactions in Familiar Object Recognition

Gamma-band responses (GBRs) are hypothesized to reflect neuronal synchronous activity related to activation of object representations. However, it is not known whether synchrony in the gamma range is also related to multisensory object processing. We investigated the effect of semantic congruity between auditory and visual information on the human GBR. The paradigm consisted of a simultaneous presentation of pictures and vocalizations of animals, which were either congruent or incongruent. EEG was measured in 17 students while they attended either the auditory or the visual stimulus and performed a recognition task. Behavioral results showed a congruity effect, indicating that information from the unattended modality affected behavior. Irrelevant visual information affected auditory recognition more than irrelevant auditory information affected visual recognition, suggesting a bias toward reliance on visual information in object recognition. Whereas the evoked (phase-locked) GBR was unaffected by congruity, the induced (non-phase-locked) GBR was increased for congruent compared with incongruent stimuli. This effect was independent of the attended modality. The results show that integration of information across modalities, based on semantic congruity, is associated with enhanced synchronized oscillations at the gamma band. This suggests that gamma-band oscillations are related not only to low-level unimodal integration but also to the formation of object representations at conceptual multisensory levels.

Continuous Flash Suppression Modulates Cortical Activity in Early Visual Cortex

A salient visual stimulus can be rendered invisible by presenting it to one eye while flashing a mask to the other eye. This procedure, called continuous flash suppression (CFS), has been proposed as an ideal way of studying awareness as it can make a stimulus imperceptible for extended periods of time. Previous studies have reported robust suppression of cortical activity in higher visual areas during CFS, but the role of primary visual cortex (V1) is still controversial. In this study, we resolve this controversy on the role of V1 in CFS and also begin characterizing the computational processes underlying CFS. Early visual cortical activity was measured with functional magnetic resonance imaging while human subjects viewed stimuli composed of target and mask, presented to the same or different eyes. Functional MRI responses in early visual cortex were smaller when target and mask were in different eyes compared with the same eye, not only for the lowest contrast target rendered invisible by CFS, but also for higher contrast targets, which were visible even when presented to the eye opposite the mask. We infer that CFS is based on modulating the gain of neural responses, akin to reducing target contrast.

The dog’s meow: asymmetrical interaction in cross-modal object recognition

Little is known on cross-modal interaction in complex object recognition. The factors influencing this interaction were investigated using simultaneous presentation of pictures and vocalizations of animals. In separate blocks, the task was to identify either the visual or the auditory stimulus, ignoring the other modality. The pictures and the sounds were congruent (same animal), incongruent (different animals) or neutral (animal with meaningless stimulus). Performance in congruent trials was better than in incongruent trials, regardless of whether subjects attended the visual or the auditory stimuli, but the effect was larger in the latter case. This asymmetry persisted with addition of a long delay after the stimulus and before the response. Thus, the asymmetry cannot be explained by a lack of processing time for the auditory stimulus. However, the asymmetry was eliminated when low-contrast visual stimuli were used. These findings suggest that when visual stimulation is highly informative, it affects auditory recognition more than auditory stimulation affects visual recognition. Nevertheless, this modality dominance is not rigid; it is highly influenced by the quality of the presented information.

Spontaneous microsaccades reflect shifts in covert attention

Microsaccade rate during fixation is modulated by the presentation of a visual stimulus. When the stimulus is an endogenous attention cue, the ensuing microsaccades tend to be directed toward the cue. This finding has been taken as evidence that microsaccades index the locus of spatial attention. But the vast majority of microsaccades that subjects make are not triggered by visual stimuli. Under natural viewing conditions, spontaneous microsaccades occur frequently (2–3 Hz), even in the absence of a stimulus or a task. While spontaneous microsaccades may depend on low-level visual demands, such as retinal fatigue, image fading, or fixation shifts, it is unknown whether their occurrence corresponds to changes in the attentional state. We developed a protocol to measure whether spontaneous microsaccades reflect shifts in spatial attention. Human subjects fixated a cross while microsaccades were detected from streaming eye-position data. Detection of a microsaccade triggered the appearance of a peripheral ring of grating patches, which were followed by an arrow (a postcue) indicating one of them as the target. The target was either congruent or incongruent (opposite) with respect to the direction of the microsaccade (which preceded the stimulus). Subjects reported the tilt of the target (clockwise or counterclockwise relative to vertical). We found that accuracy was higher for congruent than for incongruent trials. We conclude that the direction of spontaneous microsaccades is inherently linked to shifts in spatial attention.

Response to Letter: Melloni et al., “Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades.” Neuron 58, 429–441

Empirical science is about seriously considering (and possibly ruling out) alternative explanations for a given phenomenon. It is within this framework that this discussion should be addressed. Seminal intracortical work by Singer and colleagues suggested that neurons responding to stimuli which are bound, e.g., by Gestalt laws, not only display a persistent oscillation (i.e., periodic activity) in the gamma range, but also synchronize the phase of these fluctuations with each other (Gray et al., 1989).

Prestimulus Inhibition of Saccades in Adults With and Without Attention-Deficit/Hyperactivity Disorder as an Index of Temporal Expectations

Knowing when to expect important events to occur is critical for preparing context-appropriate behavior. However, anticipation is inherently complicated to assess because conventional measurements of behavior, such as accuracy and reaction time, are available only after the predicted event has occurred. Anticipatory processes, which occur prior to target onset, are typically measured only retrospectively by these methods. In this study, we utilized a novel approach for assessing temporal expectations through the dynamics of prestimulus saccades. Results showed that saccades of neurotypical participants were inhibited prior to the onset of stimuli that appeared at predictable compared with less predictable times. No such inhibition was found in most participants with attention-deficit/hyperactivity disorder (ADHD), and particularly not in those who experienced difficulties in sustaining attention over time. These findings suggest that individuals with ADHD, especially those with sustained-attention deficits, have diminished ability to benefit from temporal predictability, and this could account for some of their context-inappropriate behaviors.

Temporal dynamics of saccades explained by a self-paced process

Sensory organs are thought to sample the environment rhythmically thereby providing periodic perceptual input. Whisking and sniffing are governed by oscillators which impose rhythms on the motor-control of sensory acquisition and consequently on sensory input. Saccadic eye movements are the main visual sampling mechanism in primates, and were suggested to constitute part of such a rhythmic exploration system. In this study we characterized saccadic rhythmicity, and examined whether it is consistent with autonomous oscillatory generator or with self-paced generation. Eye movements were tracked while observers were either free-viewing a movie or fixating a static stimulus. We inspected the temporal dynamics of exploratory and fixational saccades and quantified their first-order and high-order dependencies. Data were analyzed using methods derived from spike-train analysis, and tested against mathematical models and simulations. The findings show that saccade timings are explained by first-order dependencies, specifically by their refractory period. Saccade-timings are inconsistent with an autonomous pace-maker but are consistent with a “self-paced” generator, where each saccade is a link in a chain of neural processes that depend on the outcome of the saccade itself. We propose a mathematical model parsimoniously capturing various facets of saccade-timings, and suggest a possible neural mechanism producing the observed dynamics.

Suppressive interactions underlying visually evoked fixational saccades.

Small saccades occur frequently during fixation, and are coupled to changes in visual stimulation and cognitive state. Neurophysiologically, fixational saccades reflect neural activity near the foveal region of a continuous visuomotor map. It is well known that competitive interactions between neurons within visuomotor maps contribute to target selection for large saccades. Here we asked how such interactions in visuomotor maps shape the rate and direction of small fixational saccades. We measured fixational saccades during periods of prolonged fixation while presenting pairs of visual stimuli (parafoveal: 0.8° eccentricity; peripheral: 5° eccentricity) of various contrasts. Fixational saccade direction was biased toward locations of parafoveal stimuli but not peripheral stimuli, ∼100-250ms following stimulus onset. The rate of fixational saccades toward parafoveal stimuli (congruent saccades) increased systematically with parafoveal stimulus contrast, and was suppressed by the simultaneous presentation of a peripheral stimulus. The suppression was best characterized as a combination of two processes: a subtractive suppression of the overall fixational saccade rate and a divisive suppression of the direction bias. These results reveal the nature of suppressive interactions within visuomotor maps and constrain models of the population code for fixational saccades.

Just look away: Gaze aversions as an overt attentional disengagement mechanism

During visual exploration of a scene, the eye-gaze tends to be directed toward more salient image-locations, containing more information. However, while performing non-visual tasks, such information-seeking behavior could be detrimental to performance, as the perception of irrelevant but salient visual input may unnecessarily increase the cognitive-load. It would be therefore beneficial if during non-visual tasks, eye-gaze would be governed by a drive to reduce saliency rather than maximize it. The current study examined the phenomenon of gaze-aversion during non-visual tasks, which is hypothesized to act as an active avoidance mechanism. In two experiments, gaze-position was monitored by an eye-tracker while participants performed an auditory mental arithmetic task, and in a third experiment they performed an undemanding naming task. Task-irrelevant simple motion stimuli (drifting grating and random dot kinematogram) were centrally presented, moving at varying speeds. Participants averted their gaze away from the moving stimuli more frequently and for longer proportions of the time when the motion was faster than when it was slower. Additionally, a positive correlation was found between the tasks difficulty and this aversion behavior. When the task was highly undemanding, no gaze aversion behavior was observed. We conclude that gaze aversion is an active avoidance strategy, sensitive to both the physical features of the visual distractions and the cognitive load imposed by the non-visual task.