Fixation Offset Effect Research Articles

Age differences in inhibitory and working memory functioning: limited evidence of system interactions

ABSTRACT Debate persists regarding the nature of age-related deficits in inhibition, and whether inhibitory functioning depends on working memory systems. The current research aimed to measure age-related differences in inhibition and working memory, characterize the relationship between inhibitory functions and working memory performance, and determine how these relationships are affected by age. Toward these ends, we measured performance on a range of established paradigms in 60 young adults (18–30 years) and 60 older adults (60–88 years). Our findings support age-related increases in reflexive inhibition (based on the fixation offset effect and inhibition of return) and age-related decrements in volitional inhibition (based on several paradigms: antisaccade, Stroop, flanker, and Simon). This evidence of stronger reflexive inhibition combined with weaker volitional inhibition suggests that age-related deterioration of cortical structures may allow subcortical structures to operate less controlled. Regarding working memory, older adults had lower backward digit scores and lower forward and backward spatial scores. However, of the 32 analyses (16 in each age group) that tested for dependence of inhibitory functioning on working memory functioning, only one (in young adults) indicated that inhibition performance significantly depended on working memory performance. These results indicate that inhibition and working memory function largely independently in both age groups, and age-related working memory difficulties cannot account for age-related declines in inhibitory control.

Impaired control of the oculomotor reflexes in Parkinson's disease

To investigate the role of the basal ganglia in integrating voluntary and reflexive behaviour, the current study examined the ability of patients with Parkinson's disease to voluntarily control oculomotor reflexes. We measured the size of the fixation offset effect (the reduction in saccadic reaction time when a fixation point is removed) during a block of pro- and a block of anti-saccades. Healthy controls showed the expected reduction of the FOE during the anti-saccades, which results from efforts to suppress reflexive eye movements (a preparatory set characterized by increased internal control and reduced external control). However, there was no reduction of the FOE in the anti-saccade task in Parkinson's patients, indicating that they are impaired in exerting control over oculomotor reflexes.

Fixation offset and stop signal intensity effects on saccadic countermanding: a crossmodal investigation

Two experiments utilized the stop signal paradigm to examine whether fixation offset and stop signal intensity influenced saccadic inhibition. There was a robust fixation offset effect on saccadic latencies. However, contrary to expectations, fixation offset did not influence saccadic inhibition latencies. Importantly, saccadic inhibition latencies were found to be influenced by stop signal salience, with a more intense signal leading to faster stopping. This pattern of results was observed whether the stop signal was presented in the visual or auditory modality. The results provide new insights into the mechanisms of inhibition and help resolve previous inconsistencies in the literature.

Which Visual Pathways Cause Fixation-Related Inhibition?

Visual stimuli can both inhibit and activate motor mechanisms. In one well-known example, the latency of saccadic eye movements is prolonged in the presence of a fixation stimulus, relative to the case in which the fixation stimulus disappears before the target appears. This automatic sensory-motor effect, known as the gap effect or fixation-offset effect, has been associated with inhibitory connections within the superior colliculus (SC). Visual information is provided to the SC and other oculomotor areas, such as the frontal eye fields (FEF), mainly by the magnocellular geniculostriate pathway, and also by the retinotectal pathway. We tested whether signals in these pathways are necessary to create fixation-related inhibition, by using stimuli invisible to them. We found that such stimuli, visible only to short-wave-sensitive cones (S cones), do produce fixation-related inhibition (including when warning effects were equated). We also demonstrate that this fixation-related inhibition cannot be explained by residual activation of luminance pathways and must be caused by a route separate from that of luminance fixation signals. Thus there are at least two routes that cause fixation-related inhibition, and direct sensory input to the SC or FEF by the magnocellular or retinotectal pathways is not required. We discuss the implications that there may be both cortical and collicular mechanisms.

Differential effects of target probability on saccade latencies in gap and warning tasks

Saccade latencies are significantly reduced by extinguishing a foveal fixation stimulus before the appearance of a saccade target. It has been shown recently that this "fixation offset effect" (FOE) can be modulated by varying target probability. Cortico-collicular top-down effects have been assumed to mediate this strategic FOE modulation. Here, we have investigated strategic FOE modulation in 14 healthy human subjects performing gap and warning tasks. In the former task, the central fixation point was extinguished 200 ms before target onset. In the latter task, the central fixation point changed its colour 200 ms before target onset, but remained illuminated until the target appeared. Target probability was varied block-wise between 25 and 75%. In both tasks, mean latencies decreased with increasing target probability. However, in contrast with what can be expected from preceding studies, we found no differential modulation of mean latencies by target probability between tasks. Instead, we observed differential probability-dependent changes in latency distributions. In the gap task, discrete changes of saccade latencies were found, with a probability-dependent change in frequency of express and regular latencies. By contrast, in the warning task a shift of the entire latency distribution towards longer latencies with low target probability was found. We conclude that strategic modulation of saccade latencies by target probability may be mediated by two distinct neural mechanisms. Selection of either mechanism seems to depend critically on activation of the fixation system.

Covert and overt orienting to gaze direction cues and the effects of fixation offset.

We examined covert and overt orienting in response to non-predictive gaze direction cues and investigated whether the subcortical superior colliculus (SC) plays a role in this type of orienting. Participants viewed a centrally presented gazing schematic face and responded to targets appearing at gazed-at or non-gazed-at locations either by making a keypress response while maintaining central fixation or by making an eye movement to the target. For both response conditions, the fixation stimulus (the gazing face) either remained on the screen or was extinguished at the time of target presentation, a manipulation known to engage and disengage the SC. Results revealed that participants making manual responses oriented covertly to the gazed-at location regardless of the fixation condition, and that participants making eye movements oriented overtly only if the fixation stimulus remained on the screen. Overt gaze-triggered orienting was not enhanced relative to covert orienting, and the fixation offset effect was not reduced for averted gaze cues relative to straight gaze cues. These findings suggest that gaze direction cues do not activate or predisengage the oculomotor system, and thus that orienting to gaze direction does not engage the SC. This is consistent with the view that gaze-triggered orienting is a unique form of reflexive orienting that depends crucially on cortical processes.

Contextual abnormalities of saccadic inhibition in children with attention deficit hyperactivity disorder.

Abnormalities of executive function are observed consistently in children with attention-deficit hyperactivity disorder (ADHD), and it is hypothesised that these arise because of disruption to a behavioural inhibition system. Executive and inhibitory functions were compared between unmedicated and medicated children with ADHD (combined type), age-matched healthy children and healthy adults. Executive functions were measured using a test of spatial working memory shown previously to be sensitive to ADHD and to stimulant medication. Inhibitory functions were measured using an ocular motor paradigm that required individuals to use task context to control the release of fixation. Context was set according to the probability that a target would appear at either of the two locations. In one block, targets appeared on 80% of trials. In the other block, targets appeared on 20% of trials. The ability to control the release of fixation was inferred from the fixation offset effect (FOE), or the difference in saccade latency when the current fixation is offset 200 ms prior to the onset of the saccade target (gap condition), compared with when there is no offset (overlap condition). Although the healthy children made more errors on the spatial working memory task than the healthy adults, there was no difference between the two groups in their ability to control fixation using context. Both showed a larger FOE when target probability was low. As expected, the unmedicated ADHD group made more errors on the spatial working memory test than the healthy children, although spatial working memory performance was normal in the medicated ADHD group. However, both the unmedicated and medicated ADHD groups were unable to modulate the FOE according to context, and this was due to their inability to voluntarily inhibit saccades when there was a low target probability. These data suggest that the context-based modulation of fixation release is not controlled by the same systems that control executive function. Furthermore, deficits in executive function and inhibitory control appear independent in children with ADHD.

Control of eye movement reflexes.

We investigated the effect of strategic suppression of reflexive eye movements on external control over fixation using a fixation offset paradigm. A visual signal at fixation facilitates the fixation reflex and inhibits eye movements. Certain preparatory states render the fixation reflex less reactive to visual stimulation at fixation, as evidenced by a reduction in the fixation offset effect (FOE). For example, past studies have suggested that the reduced FOE during anti-saccade tasks results from the requirement to inhibit reflexive eye movements. We tested whether suppressing reflexive saccades reduces external control over ocular fixation using a go-nogo saccade paradigm. During each trial, one of two targets appeared in the periphery. Participants were instructed to saccade to one target (go), but when the other target appeared they either had to maintain fixation (nogo) or move their eyes in the direction opposite the target (anti). When nogo trials were admixed with target-directed saccades a large FOE was observed compared to when target-directed saccades occurred alone (experiment 1); however, when anti-saccades were mixed with target-directed saccades, a small FOE was observed for both types of eye movements (experiment 2). We conclude that suppressing reflexive eye movements does not reduce external control over fixation. Further research is necessary to elucidate which other component of preparing to make an anti-saccade diminishes the FOE.

Strategic control over saccadic eye movements: studies of the fixation offset effect.

We studied the strategic (presumably cortical) control of ocular fixation in experiments that measured the fixation offset effect (FOE) while manipulating readiness to make reflexive or voluntary eye movements. The visual grasp reflex, which generates reflexive saccades to peripheral visual signals, reflects an opponent process in the superior colliculus (SC) between fixation cells at the rostral pole, whose activity helps maintain ocular position and increases when a stimulus is present at fixation, and movement cells, which generate saccades and are inhibited by rostral fixation neurons. Voluntary eye movements are controlled by movement and fixation cells in the frontal eye field (FEF). The FOE--a decrease in saccade latency when the fixation stimulus is extinguished--has been shown to reflect activity in the collicular eye movement circuitry and also to have an activity correlate in the FEF. Our manipulation of preparatory set to make reflexive or voluntary eye movements showed that when reflexive saccades were frequent and voluntary saccades were infrequent, the FOE was attenuated only for reflexive saccades. When voluntary saccades were frequent and reflexive saccades were infrequent, the FOE was attenuated only for voluntary saccades. We conclude that cortical processes related to task strategy are able to decrease fixation neuron activity even in the presence of a fixation stimulus, resulting in a smaller FOE. The dissociation in the effects of a fixation stimulus on reflexive and voluntary saccade latencies under the same strategic set suggests that the FOEs for these two types of eye movements may reflect a change in cellular activity in different neural structures, perhaps in the SC for reflexive saccades and in the FEF for voluntary saccades.

Estimating the components of the gap effect.

The gap effect refers to the finding that saccadic latencies are typically reduced when a fixation point is removed prior to the appearance of a peripheral target. This reduction in saccadic reaction time (SacRT) is thought to be due to a general warning effect and an oculomotor specific fixation offset that occur when the fixation point is removed. In order to estimate the contribution of each of these effects to the overall gap effect, this paper introduces a new manipulation, the partial-gap trial, where the fixation point undergoes a change in size prior to the presentation of the target. The partial-gap trial is presumed to provide the visual warning effect of the fixation offset (i.e. similar to that in a gap trial) but does not provide the fixation offset effect (FOE). When the fixation point was abruptly reduced in size before the presentation of the target, the estimated decrease in SacRT due to the visual warning effect was 5-7% and did not differ in the presence or absence of an auditory warning signal. It was found that auditory warning effect and the FOE interacted in reducing SacRTs. Additionally, when the fixation point was abruptly increased in size before the presentation of the target, SacRTs were slower than when the fixation point did not change in size and remained present for the entire trial (i.e. an overlap trial). We conclude that this new partial-gap paradigm is a useful method for researchers wishing to separately examine FOE and visual warning effects.

The Magnitude of the Fixation Offset Effect with Endogenously and Exogenously Controlled Saccades

Two experiments examined saccadic reaction time (RT) in response to visual targets as a function of fixation offset condition (no offset; target simultaneous with offset and 200-msec offset-target SOA) in prosaccade and antisaccade tasks. The second experiment also included a condition in which saccades were made in response to verbal commands presented auditorally. To ensure that observers were equally prepared in each condition, auditory warning tones preceded target onset on every trial. The RT reduction associated with fixation offset (FOE, or gap effect) was identical with visual targets in the prosaccade task and in response to verbal signals, strongly implicating motor, rather than sensory, mechanisms in the FOE. The FOE in the antisaccade task was significant, but it was also significantly smaller than in the other tasks. We speculate that the reduced FOE in the antisaccade task may be due to the requirement to inhibit the superior colliculus when the target directed saccadic programs are, by instruction, erroneous.

Visual offsets facilitate saccadic latency: does predisengagement of visuospatial attention mediate this gap effect?

Saccadic reaction time (RT) is reduced when a fixation stimulus is extinguished 200 ms before a target appears. An attentional predisengagement theory (APT) may explain this gap effect: When covert attention is engaged (e.g., on fixation), the saccadic system is inhibited and RT is delayed; when the attended stimulus is extinguished, attention is disengaged, the inhibition is removed, and RT is facilitated. In 3 experiments covert attention was endogenously or exogenously cued to an object on the vertical meridian. Onset of a saccadic target on the horizontal meridian could be preceded by the offset of an attended or unattended object. Contrary to APT, RTs were identical after attended and unattended offsets. Results suggest that the gap effect has 2 components, and covert visual attention plays no role. One component is motor system preparation; the other is a fixation offset effect specific to the oculomotor system.