Two mechanisms underlying inhibition of return

Inhibition of return (IOR) refers to slower reaction times to targets presented at previously stimulated or inspected locations. Taylor and Klein (J Exp Psychol Hum Percept Perform 26(5):1639–1656, 2000) showed that IOR can affect either attentional/perceptual or motor processes, depending on whether the oculomotor system is in a quiescent or in an activated state, respectively. If the motoric flavour of IOR is truly non-perceptual and non-attentional, no IOR should be observed when the responses to targets are not based on spatial information. In the present experiments, we demonstrated that when the eyes moved to the peripheral cue and back to centre before the target appeared (to generate the motoric flavour), IOR was observed in detection tasks, for which the spatial location is an integral feature of the onset that is reported, but not in colour discrimination tasks, for which the outcome of a non-spatial perceptual discrimination is reported. When eye movements were prevented, both tasks showed robust IOR. We, therefore, conclude that the motoric flavour of IOR, elicited by oculomotor activation, does not affect attention or perceptual processing.     

"Motor oblique effect": perceptual direction discrimination and pointing to memorized visual targets share the same preference for cardinal orientations

In previous studies we observed a pattern of systematic directional errors when humans pointed to memorized visual target locations in two-dimensional (2-D) space. This directional error was also observed in the initial direction of slow movements toward visual targets or movements to kinesthetically defined targets in 2-D space. In this study we used a perceptual experiment where subjects decide whether an arrow points in the direction of a visual target in 2-D space and observed a systematic distortion in direction discrimination known as the "oblique effect." More specifically, direction discrimination was better for cardinal directions than for oblique. We then used an equivalent measure of direction discrimination in a task where subjects pointed to memorized visual target locations and showed the presence of a motor oblique effect. We finally modeled the oblique effect in the perceptual and motor task using a quadratic function. The model successfully predicted the observed direction discrimination differences in both tasks and, furthermore, the parameter of the model that was related to the shape of the function was not different between the motor and the perceptual tasks. We conclude that a similarly distorted representation of target direction is present for memorized pointing movements and perceptual direction discrimination.     

Perceptual priming does not transfer interhemispherically in the acallosal brain

Acallosal participants usually do not display any disconnection signs in tasks requiring an explicit or declarative type of response. They can accurately compare stimuli placed in each hand and they perform normally on lateralized recognition tasks. They, however, show impairment in tasks assessing interdependent motor control, bilateral coordination and they are also unable to intermanually transfer an implicit procedural motor skill. These deficits suggest that compensation might be limited when a motor component is involved. Alternately, it is also possible that interhemispheric transmission in callosal agenesis might be limited when implicit or unconscious processes are involved (Berlucchi et al. in Neuropsychologia 33:923–936, 1995; De Guise et al. in Brain 122:1049–1062, 1999). The aim of the present study was to assess interhemispheric transfer in two distinct nondeclarative tasks, namely visuoperceptual skill learning and perceptual priming, with a lateralized version of the fragmented picture task developed by Snodgrass et al. (Behav Res Methods Inst Comp 19:270–274, 1987) that did not involve any motor component. The performance of five acallosal and one early-callosotomized individuals was compared to that of control participants divided into four groups (n = 10) according to which hemisphere was trained (left or right) and which response mode was used (manual or verbal). Visuoperceptual skill learning was observed in all control groups except for the group submitted to training of the left hemisphere in the manual modality of response. The acallosal and early-callosotomized participants did not show any implicit learning of the visuoperceptual skill on any of the conditions. The evaluation of the perceptual priming effect in the second part of the testing revealed that the priming effect was restricted to the trained hemisphere in participants without corpus callosum, as opposed to all neurogically intact participants who presented interhemispheric transfer of the priming effect. These findings indicate that the compensatory pathways, most probably subcortical commissures, are insufficient to allow interhemispheric transfer of perceptual priming, confirming the limits of neural plasticity in the absence of the corpus callosum. They also support the dissociation between declarative and nondeclarative memory in the split-brain and acallosal participants suggested by Berlucchi et al. (1995) and observed by De Guise et al. (Brain 122:1049–1062, 1999). These results are further discussed within the context of neurobiological theories of memory systems.     

Inhibition of return in cue–target and target–target tasks

Inhibition of return (IOR), the term given for the slowing of a response to a target that appeared at the same location as a previously presented stimulus, has been studied with both target–target (TT; participants respond to each successive event) and cue–target (CT; participants only respond to the second of two events) tasks. Although both tasks have been used to examine the processes and characteristics of IOR, few studies have been conducted to understand if there are any differences in the processes that underlie the IOR that results from ignoring (CT paradigm) or responding to (TT paradigm) the first stimulus. The purpose of the present study was to examine the notion that IOR found in TT tasks represents “true” IOR whereas IOR found in CT tasks consist of both “true” IOR and response inhibition (Coward et al. in Exp Brain Res 155:124–128, 2004). Consistent with the pattern of effects found by Coward et al. (Exp Brain Res 155:124–128, 2004), IOR was larger in the CT task than in the TT task when a single detection response was required (Experiment 1). However, when participants completed one of two spatially-directed responses (rapid aiming movement to the location of the target stimulus), IOR effects from the CT and TT tasks were equal in magnitude (Experiment 2). Rather than CT tasks having an additional response inhibition component, these results suggest that TT tasks may show less of an inhibitory effect because of a facilitatory response repetition effect.     

Observing human interaction with physical devices

Triggering of saccades depends on the task: in the gap task, fixation point switches off and target appears after a gap period; in the overlap task, target appears while fixation point is still on. Saccade latencies are shorter in the gap task, due to fixation disengagement and advanced movement preparation during the gap. The two modes of initiation are also hypothesized to be subtended by different cortical-subcortical circuits. This study tested whether interleaving the two tasks modifies latencies, due to switching between different modes of triggering. Two groups of healthy participants (21–29 vs. 39–55 years) made horizontal and vertical saccades in gap, overlap, and mixed tasks; saccades were recorded with the Eyelink. Both groups showed shorter latencies in the gap task, i.e. a robust gap effect and systematic differences between directions. For young adults, interleaving tasks made the latencies shorter or longer depending on direction, while for middle-age adults, latencies became longer for all directions. Our observations can be explained in the context of models such as that of Brown et al. (Neural Netw 17:471–510, 2004), which proposed that different combinations of frontal eye field (FEF) layers, interacting with cortico-subcortical areas, control saccade triggering in gap and overlap trials. Moreover, we suggest that in early adulthood, the FEF is functioning optimally; frequent changes of activity in the FEF can be beneficial, leading to shorter latencies, at least for some directions. However, for middle-age adults, frequent changes of activity of a less optimally functioning FEF can be time consuming. Studying the alternation of gap and overlap tasks provides a fine tool to explore development, aging and disease. M. Vernet and Z. Kapoula contributed equally to this work.     

Grasp effects of the Ebbinghaus illusion are ambiguous

The assumption that the Ebbinghaus/Titchener illusion deceives perception but not grasping, which would confirm the two-visual-systems hypothesis (TVSH) as proposed by Milner and Goodale (The visual brain in action, 1995), has recently been challenged. Franz et al. (Exp Brain Res 149:470–477, 2003) found that the illusion affects both perception and grasping, and showed that the effect of the illusion on the peak grip aperture (PGA) cannot be accounted for by different sizes of the gap that separates the central target disk from the surrounding flankers. However, it is not yet clear if the presence of flankers per se influences grasping. We therefore compared kinematic parameters of prehension, using the Ebbinghaus illusion, and a neutral control condition where normal subjects grasped a disk without any flankers. In accordance with the well-known effects of the illusion on perceived size, the PGA was smaller when the target disk was surrounded by large flankers, and larger when it was encircled by small flankers. However, the largest PGA values were reached in the neutral control condition. Hence the presence of flankers leads to a general reduction of the PGA, possibly because the flankers are regarded as obstacles. This ‘reduction effect’ casts doubts on how appropriate it is to directly compare perceptual measures and PGA values when using the Ebbinghaus illusion. Even smaller effects of the illusion on the PGA compared to larger perceptual effects cannot be unequivocally interpreted.     

Dual LATER-unit model predicts saccadic reaction time distributions in gap, step and appearance tasks

Saccadic latencies have long been known to depend on the relative timing of the appearance of the new target, and offset of the original fixation target. Previous studies have tended to conclude that two separate effects are at work, one equivalent to competitive inhibition from the fixation target, and the other due to its offset providing a warning that shortens latency. In this study, we propose a simpler explanation, based on a well-established model of reaction time, LATER (linear approach to threshold with ergodic rate), that in addition to predicting mean latencies also—more challengingly—predicts latency distributions. We show that observed distributions, using gap, step and appearance tasks under three conditions of prior probability, can be accurately predicted by using a pair of LATER units, one corresponding to fixation target offset and the other to peripheral target onset. Because fixation offset is probabilistically associated with target appearance, when the fixation unit is activated it increases the target’s decision signal (that represents probability) in a fixed proportion, speeding responses. In contrast, when the fixation target remains present, the fixation unit is not activated, and responses are slower. Both these effects generate characteristic changes in the shapes of the latency distributions that can be accurately predicted by the model.     

Visuomotor dependency on an initial fixation target involved in the disorder of visually-guided manual movement in Parkinson's disease

Role of a central fixation target on the latencies of visually guided manual movement was analyzed on young healthy subjects, age-matched control subjects and patients with Parkinson's disease (Hoehn and Yahr stages II, III, and IV). Two paradigms were used: overlap paradigm where a central fixation target was lighted throughout the test, and gap paradigm where a central fixation target was turned off 200 ms before a peripheral target was lighted. The subject was first asked to fixate the central target then instructed to locate a peripheral target with a laser beam spot, operated with wrist flexion or extension as quickly as possible. Latencies of gap paradigm are always shorter than those of overlap task in all the groups. Latencies of both overlap and gap tasks prolonged from young to elder, from elder to PD II, from PD II to PD III and from PD III to PD IV. Also latencies were extremely prolonged in the overlap tasks and correlated with disease severity. Latencies in the gap tasks were less prolonged as compared with those in the overlap tasks. The visual fixation target prolonged the visuo-motor latency in association with severity of Parkinson's disease.     

Express saccades in cat: effects of task and target modality

Saccadic eye movements to visual, auditory, and bimodal targets were measured in four adult cats. Bimodal targets were visual and auditory stimuli presented simultaneously at the same location. Three behavioral tasks were used: a fixation task and two saccadic tracking tasks (gap and overlap task). In the fixation task, a sensory stimulus was presented at a randomly selected location, and the saccade to fixate that stimulus was measured. In the gap and overlap tasks, a second target (hereafter called the saccade target) was presented after the cat had fixated the first target. In the gap task, the fixation target was switched off before the saccade target was turned on; in the overlap task, the saccade target was presented before the fixation target was switched off. All tasks required the cats to redirect their gaze toward the target (within a specified degree of accuracy) within 500 ms of target onset, and in all tasks target positions were varied randomly over five possible locations along the horizontal meridian within the cat's oculomotor range. In the gap task, a significantly greater proportion of saccadic reaction times (SRTs) were less than 125 ms, and mean SRTs were significantly shorter than in the fixation task. With visual targets, saccade latencies were significantly shorter in the gap task than in the overlap task, while, with bimodal targets, saccade latencies were similar in the gap and overlap tasks. On the fixation task, SRTs to auditory targets were longer than those to either visual or bimodal targets, but on the gap task, SRTs to auditory targets were shorter than those to visual or bimodal targets. Thus, SRTs reflected an interaction between target modality and task. Because target locations were unpredictable, these results demonstrate that cats, as well as primates, can produce very short latency goal-directed saccades.     

“Graspability” of objects affects gaze patterns during perception and action tasks

When grasping an object, our gaze marks key positions to which the fingertips are directed. In contrast, eye fixations during perceptual tasks are typically concentrated on an object’s centre of mass (COM). However, previous studies have typically required subjects to either grasp the object at predetermined sites or just look at computer-generated shapes “as a whole”. In the current study, we investigated gaze fixations during a reaching and grasping task to symmetrical objects and compared these fixations with those made during a perceptual size estimation task using real (Experiment 1) and computer-generated objects (Experiment 2). Our results demonstrated similar gaze patterns in both perception and action to real objects. Participants first fixated a location towards the top edge of the object, consistent with index finger location during grasping, followed by a subsequent fixation towards the object’s COM. In contrast, during the perceptual task to computer-generated objects, an opposite pattern in fixation locations was observed, where first fixations were closer to the COM, followed by a subsequent fixation towards the top edge. Even though differential fixation patterns were observed between studies, the area in which these fixations occurred, between the centre of the object and top edge, was the same in all tasks. These results demonstrate for the first time consistencies in fixation locations across both perception and action tasks, particularly when the same type of information (e.g. object size) is important for the completion of both tasks, with fixation locations increasing relative to the object’s COM with increases in block height.     

Perception action interaction: the oblique effect in the evolving trajectory of arm pointing movements

In previous studies, we provided evidence for a directional distortion of the endpoints of movements to memorized target locations. This distortion was similar to a perceptual distortion in direction discrimination known as the oblique effect so we named it the “motor oblique effect”. In this report we analyzed the directional errors during the evolution of the movement trajectory in memory guided and visually guided pointing movements and compared them with directional errors in a perceptual experiment of arrow pointing. We observed that the motor oblique effect was present in the evolving trajectory of both memory and visually guided reaching movements. In memory guided pointing the motor oblique effect did not disappear during trajectory evolution while in visually guided pointing the motor oblique effect disappeared with decreasing distance from the target and was smaller in magnitude compared to the perceptual oblique effect and the memory motor oblique effect early on after movement initiation. The motor oblique effect in visually guided pointing increased when reaction time was small and disappeared with larger reaction times. The results are best explained using the hypothesis that a low level oblique effect is present for visually guided pointing movements and this effect is corrected by a mechanism that does not depend on visual feedback from the trajectory evolution and might even be completed during movement planning. A second cognitive oblique effect is added in the perceptual estimation of direction and affects the memory guided pointing movements. It is finally argued that the motor oblique effect can be a useful probe for the study of perception–action interaction.     

Dual-task costs and benefits in anti-saccade performance

It has been reported that anti-saccade performance is facilitated by diverting attention through a secondary task (Kristjánsson et al. in Nat Neurosci 4:1037–1042, 2001). This finding supports the idea that the withdrawal of resources that would be taken up by the erroneous movement plan makes it easier to overcome the tendency to look towards the imperative stimulus. We first report an attempt to replicate this finding. Four observers were extensively tested in an anti-saccade paradigm. The luminance of the fixation point or peripheral target was briefly increased or decreased. In the dual-task condition observers signalled the direction of the luminance change. In the single-task condition the discrimination stimulus was presented, but could be ignored as it required no response. We found an overall dual-task cost in anti-saccade latency, although some facilitation was observed in the accuracy. The discrepancy between the two studies was attributed to performance in the single-task condition. For latency facilitation to occur, performance should not be affected by the discrimination stimulus when it is task-irrelevant. We show that naive, untrained observers could not ignore this irrelevant visual event. If it occurred before the imperative movement signal, the event acted as a warning signal, speeding up anti-saccade generation. If it occurred after the imperative movement stimulus, it acted as a remote distractor and interfered with the generation of the correct movement. Under normal circumstances, these basic oculomotor effects operate in both single- and dual-task conditions. An overall dual-task cost rides on top of this latency modulation. This overall cost is best accounted for by an increase in the response criterion for saccade generation in the more demanding dual-task condition.     

Temporal attention shortens perceptual latency: a temporal prior entry effect

The prior entry hypothesis of attention holds that attended stimuli are perceived earlier than unattended stimuli. Whereas this speeding of perceptual processing has been repeatedly demonstrated for spatial attention, it has not been reported within the temporal domain. To fill this gap, we tested whether temporal attention accelerates auditory perceptual processing by employing event-related potentials as on-line indicators of perceptual processing. In a modified oddball paradigm, we presented a single tone in each trial, either a frequent standard tone or an infrequent deviant or target tone. Temporal attention to tones was manipulated via constant foreperiods. We observed that the latency of the N2, an event-related potential reflecting perceptual processing, is shortened by temporal attention. This result provides first evidence for the idea that temporal attention accelerates perceptual processing as suggested by the prior entry hypothesis.     

Latency of saccades during smooth-pursuit eye movement in man Directional asymmetries

To examine the effects of smooth-pursuit eye movements on the initiation of saccades, their latency was measured when subjects initially fixated or pursued a target. In half of the block of trials, the fixation or pursuit target was extinguished 200 ms before the saccade target was illuminated (gap trials). Reduction of the mean saccade latency in the gap trials (the “gap effect”) was evident even when the subjects were pursuing a moving target, consistent with previous observations. The effect of pursuit direction on saccade latency was also examined. Saccades in the same direction as the preceding pursuit (forward saccades) had shorter latencies than those in the opposite direction (backward saccades). This asymmetry was observed in both the gap and nongap trials. Although the forward-backward asymmetry was much smaller than the “gap effect”, it was statistically significant in six of eight cases. These results suggest that the preparation of saccades is affected by smooth-pursuit eye movements. Received: 2 June 1997 / Accepted: 6 November 1997     

Impaired savings despite intact initial learning of motor adaptation in Parkinson’s disease

In motor adaptation, the occurrence of savings (faster relearning of a previously learned motor adaptation task) has been explained in terms of operant reinforcement learning (Huang et al. in Neuron 70(4):787–801, 2011), which is thought to associate an adapted motor command with outcome success during repeated execution of the adapted movement. There is some evidence for deficient savings in Parkinson’s Disease (PD), which might result from deficient operant reinforcement processes. However, this evidence is compromised by limited adaptation training during initial learning and by multi-target adaptation, which reduces the number of reinforced movement repetitions for each target. Here, we examined savings in PD patients and controls following overlearning with a single target. PD patients showed less savings than controls after successive adaptation and deadaptation blocks within the same test session, as well as less savings across test sessions separated by a 24-h delay. It is argued that impaired blunted dopaminergic signals in PD impairs the modulation of dopaminergic signals to the motor cortex in response to rewarding motor outcomes, thus impairing the association of the adapted motor command with rewarding motor outcomes. Consequently, the previously adapted motor command is not preferentially selected during relearning, and savings is impaired.     

The effect of transcranial magnetic stimulation on the latencies of vertical saccades

In this study, we investigated the effect of transcranial magnetic stimulation (TMS) over the right posterior parietal cortex (PPC) on the latency of two different types of visually-guided vertical saccades: reflexive saccades triggered by the sudden onset of a target, and saccades towards target locations known in advance. For this reason, we used two oculomotor tasks: a gap and a delay task, respectively. Nine normal subjects performed vertical saccades at ±7.5 and ±15°. TMS was applied at 80 and 100 ms after target onset in the gap task, and after fixation offset in the delay task. Without TMS, we confirmed a latency asymmetry in the gap task favouring upward saccades at the lower eccentricity (7.5°), and a latency symmetry in the delay task. TMS increased the latencies of all saccades in the delay task, when delivered at 100 ms. This effect was mostly pronounced for downward saccades at 7.5°. As a result, saccade latencies showed an asymmetry in this condition, similar to the one observed in the gap task without TMS. The gap task with TMS resulted in a variable latency distribution and no significant overall effect on saccade latency. Our results indicate that the right PPC is involved in the initiation of vertical saccades in the delay task, and that this involvement appears to be enhanced for downward saccades. A conclusion for the involvement of this area in the gap task could not be drawn from this study.     

Fixation disengagement enhances peripheral perceptual processing: evidence for a perceptual gap effect

Temporal gaps between the offset of a central fixation stimulus and the onset of an eccentric target typically reduce saccade latencies (saccadic gap effect). Here, we test whether temporal gaps also affect perceptual performance in peripheral vision. In Experiment 1, subjects executed saccades to briefly presented peripheral target letters and reported letter identity afterwards. A central fixation stimulus either remained visible throughout the trial (overlap) or disappeared 200 ms before letter onset (gap). Experiment 2 tested perceptual performance without saccade execution, whereas Experiment 3 tested saccade execution without perceptual demands. Peripheral letter perception performance was enhanced in gap as compared to overlap conditions (perceptual gap effect) irrespective of concurrent oculomotor demands. Furthermore, the saccadic gap effect was modulated by concurrent perceptual demands. Experiment 4 ruled out a general warning explanation of the perceptual gap effect. These findings extend recent theories assuming a strong coupling between the preparation of goal-directed saccades and shifts of visual attention from the spatial to the temporal domain.     

Influence of removal of invisible fixation on the saccadic and manual gap effect

Saccadic and manual reactions to a peripherally presented target are facilitated by removing a central fixation stimulus shortly before a target onset (the gap effect). The present study examined the effects of removal of a visible and invisible fixation point on the saccadic gap effect and the manual gap effect. Participants were required to fixate a central fixation point and respond to a peripherally presented target as quickly and accurately as possible by making a saccade (Experiment 1) or pressing a corresponding key (Experiment 2). The fixation point was dichoptically presented, and visibility was manipulated by using binocular rivalry and continuous flash suppression technique. In both saccade and key-press tasks, removing the visible fixation strongly quickened the responses. Furthermore, the invisible fixation, which remained on the display but suppressed, significantly delayed the saccadic response. Contrarily, the invisible fixation had no effect on the manual task. These results indicate that partially different processes mediate the saccadic gap effect and the manual gap effect. In particular, unconscious processes might modulate an oculomotor-specific component of the saccadic gap effect, presumably via subcortical mechanisms.     

Reaction times of manual responses to a visual stimulus at the goal of a planned memory-guided saccade in the monkey

Monkeys demonstrate improved contrast sensitivity at the goal of a planned memory-guided saccade (Science 299:81–86, 2003). Such perceptual improvements have been ascribed to an endogenous attentional advantage induced by the saccade plan. Speeded reaction times have also been used as evidence for attention. We therefore asked whether the attentional advantage at the goal of a planned memory-guided saccade led to speeded manual reaction times following probes presented at the saccade goal in a simple detection task. We found that monkeys showed slower manual reaction times when the probe appeared at the memorized goal of the planned saccade when compared to manual reaction times following a probe that appeared opposite the saccade goal. Flashing a distractor at the saccade goal after target presentation appeared to slow reaction times further. Our data, combined with prior results, suggest that a spatially localized inhibition operates on the neural representation of the saccade goal. This inhibition may be closely related or identical to the processes underlying inhibition-of-return. We also found that if the same detection task was interleaved with a difficult perceptual discrimination task, manual reaction times became faster when the probe was at the saccade goal. We interpret these results as being an effect of task difficulty; the more difficult interleaved task may have engaged endogenous attentional resources more effectively, allowing it to override the inhibition at the saccade goal. We construct and discuss a simple working hypothesis for the relationship between the effects of prior attention on neural activity in salience maps and on performance in detection and discrimination tasks.