During natural viewing, neural processing of visual targets continues throughout saccades

Relatively little is known about visual processing during free-viewing visual search in realistic dynamic environments. Free-viewing is characterized by frequent saccades. During saccades, visual processing is thought to be inhibited, yet we know that the pre-saccadic visual content can modulate post-saccadic processing. To better understand these processes in a realistic setting, we study here saccades and neural responses elicited by the appearance of visual targets in a realistic virtual environment. While subjects were being driven through a 3D virtual town they were asked to discriminate between targets that appear on the road. We found that the presence of a target enhances early occipital as well as late frontocentral saccade-related responses. The earlier potential, shortly after 125ms post-saccade onset, was enhanced for targets that appeared in peripheral vision as compared to central vision, suggesting that fast peripheral processing initiated before saccade onset. The later potential, at 195ms post-saccade onset, was strongly modulated by the visibility of the target with a spatial distribution reminiscent of the classic P300 response. Together these results suggest that, during natural viewing, neural processing of the pre-saccadic visual stimulus continues throughout the saccade, apparently unencumbered by saccadic inhibition.

EXPRESS: Distraction by auditory novelty during reading: Evidence for disruption in saccade planning, but not saccade execution

Novel or unexpected sounds that deviate from an otherwise repetitive sequence of the same sound cause behavioural distraction. Recent work has suggested that distraction also occurs during reading as fixation durations increased when a deviant sound was presented at the fixation onset of words. The present study tested the hypothesis that this increase in fixation durations occurs due to saccadic inhibition. This was done by manipulating the temporal onset of sounds relative to the fixation onset of words in the text. If novel sounds cause saccadic inhibition, they should be more distracting when presented during the second half of fixations when saccade programming usually takes place. Participants read single sentences and heard a 120 ms sound when they fixated five target words in the sentence. On most occasions (p= 0.9), the same sine wave tone was presented (“standard”), while on the remaining occasions (p= 0.1) a new sound was presented (“novel”). Critically, sounds were played either during the first half of the fixation (0 ms delay) or during the second half of the fixation (120 ms delay). Consistent with the saccadic inhibition hypothesis, novel sounds led to longer fixation durations in the 120 ms compared to the 0 ms delay condition. However, novel sounds did not generally influence the execution of the subsequent saccade. These results suggest that unexpected sounds have a rapid influence on saccade planning, but not saccade execution.

Involuntary Markers of Saliency and Surprise Revealed by Oculomotor Inhibition in Response to Auditory Sequences

Our eyes move constantly but are often inhibited momentarily in response to external stimuli. The properties of this Oculomotor-Inhibition (OMI) depend on the stimulus saliency, anticipation, and attention. Previous studies have shown prolonged saccadic inhibition for auditory oddballs; however, they required active counting of the oddballs. Here we investigated whether the OMI response to auditory deviants can provide a quantitative measure of deviance strength (auditory pitch difference) and investigated its dependence on the Inter-Stimulus Interval (ISI), without requesting a voluntary attention to the deviant stimulus. Observers fixated on a central fixation stimulus and passively listened to repeated short sequences of pure tones that contained a deviant tone either regularly or with 20% probability (the Oddball paradigm). The results showed, as in previous studies, prolonged microsaccade inhibition following the deviant tone. Moreover, the inhibition onset latency was shorter in proportion to the pitch deviance (the saliency effect) and the release was significantly longer for rare deviants (the surprise effect) as long as the ISI was short (<2.5s). Taken together, these results suggest that OMI provides involuntary markers of saliency and surprise, which can be obtained without the observer’s response.

Time-locked inhibition of covert orienting

It is well known that visual transients can abolish the execution of an eye movement about 90 ms later, a phenomenon known as saccadic inhibition (SI). But it is not known if the same inhibitory process might influence covert orienting in the absence of saccades, and consequently alter visual perception. We measured orientation discrimination performance in 14 participants during a covert orienting task (modified Posner paradigm) in which an uninformative exogenous visual cue preceded the onset of an oriented probe stimulus by 120 to 306 ms. In half of the trials the onset of the probe was accompanied by a brief irrelevant flash, a visual transient that would normally induce SI in an overt task. We report a SI-like time-specific covert inhibition effect in which the irrelevant flash impaired orientation discrimination accuracy only when the probe followed the cue between 165 to 265 ms. The interference was more pronounced when the cue was incongruent with the probe location. We suggest that covert orienting may be susceptible to similar inhibitory mechanisms that generate SI in overt orienting, although the precise time course and mechanisms of this novel effect require further characterisation.

Spatial constraints in saccadic inhibition of return

Despite being one of the most prominent and well-known biases in visual orienting, inhibition of return (IOR), a tendency to avoid recently viewed locations, remains a controversial and poorly understood phenomenon. To investigate the characteristics of IOR, participants made rapid alternating saccades between two targets, return saccades, or produced eye movements that followed an “hourglass” pattern in which the same location was only revisited every fourth eye movement. Saccade dwell times and secondary saccade frequency increased when the eye returned immediately to a previously viewed location. Surprisingly, the higher rate of secondary saccades did not contribute directly to the longer dwell times in the return condition. Saccade precision was equivalent between conditions, but saccade gain was smaller for hourglass saccades. Varying the height and width of the hourglass revealed that the magnitude of inhibition of return depended on the angular separation between subsequent saccades and was not characterized by a constant zone around the targets. Even when the angular difference of hourglass saccades, relative to return saccades, was made as small as 3 degrees, significant differences in dwell times and secondary saccade characteristics were observed. The results further explicate constraints on inhibition of return, reveal novel factors guiding secondary saccade programming, and provide insight into motor and attentional constraints governing the rate of sequential eye movements.

Pardon the interruption: saccadic inhibition enables the rapid deployment of alternate oculomotor plans

Diverse psychophysical and neurophysiological results show that oculomotor networks are continuously active, such that plans for making the next eye movement are always ongoing. So, when new visual information arrives unexpectedly, how are those plans affected? At what point can the new information start guiding an eye movement, and how? Here, based on modeling and simulation results, we make two observations that are relevant to these questions. First, we note that many experiments, including those investigating the phenomenon known as “saccadic inhibition,” are consistent with the idea that sudden-onset stimuli briefly interrupt the gradual rise in neural activity associated with the preparation of an impending saccade. And second, we show that this stimulus-driven interruption is functionally adaptive, but only if perception is fast. In that case, putting on hold an ongoing saccade plan toward location A allows the oculomotor system to initiate a concurrent, alternative plan toward location B (where a stimulus just appeared), deliberate (briefly) on the priority of each target, and determine which plan should continue. Based on physiological data, we estimate that the actual advantage of this strategy, relative to one in which any plan once initiated must be completed, is of several tens of milliseconds.

Saccadic inhibition in a guided saccade task

The eye movement system reacts very systematically to visual transients that are presented during the planning phase of a saccade. About 50 to 70 ms after the onset of a transient, the number of saccades that are started decreases, a phenomenon that has been termed saccadic inhibition. Saccades started just before this time window are hypometric compared to regular saccades, presumably because the presentation of the transient stops them in mid-flight. Recent research investigating the properties of repeated saccades to fixed locations found that these early saccades were additionally faster than expected from the main sequence relation, suggesting that a saccadic dead time during which saccades can no longer be modified does not exist. The present study investigated the properties of saccades to random locations in a guided saccade task. As expected, early saccades starting just before the saccadic inhibition dip in frequency were hypometric. Their velocity profiles implied that these saccades were actively stopped after reaching peak velocity. However, the peak velocities of these saccades did not generally deviate from the main sequence relation. The question whether an active stop of early saccades is incompatible with the idea of a saccadic dead time is open to debate.