Exp Brain Res (2015) 233:3059–3071 DOI 10.1007/s00221-015-4374-x

RESEARCH ARTICLE

Interaction between spatial inhibition of return (IOR) and executive control in three‑dimensional space Aijun Wang1,2,4 · Zhenzhu Yue3 · Ming Zhang2 · Qi Chen1 

Received: 3 March 2015 / Accepted: 29 June 2015 / Published online: 14 July 2015 © Springer-Verlag Berlin Heidelberg 2015

Abstract  It has been well documented how spatial inhibition of return (IOR) interacts with executive functions in a two-dimensional plane, i.e., significantly decreased interference at the cued (inhibited) compared to the uncued location. It remains unknown, however, how spatial IOR interacts with executive functions along the depth dimension of the real 3D world. Here, we adapted the Posner spatialcuing paradigm into a virtual 3D world. The location-based IOR was orthogonally combined with the flanker effect: The target and its flanker could appear at either the cued or the uncued location in a closer or farther depth plane. Moreover, the flanker effect was differentiated into the preresponse and response levels, and the flankers could appear in the either same (Experiment 1) or different (Experiment 2) depth plane from the target. A simple detection task was also adopted to test the pure effect of how visuospatial attention is prevented from returning previously attended location along the depth dimension. The results showed that there existed significant IOR effects only when target was presented in the farther depth plane. Moreover, significantly reversed response-level conflicts were observed at the cued location in the farther depth plane, indicating that

* Qi Chen [email protected] 1

Center for Studies of Psychological Application and School of Psychology, South China Normal University, Guangzhou 510631, People’s Republic of China

2

Department of Psychology, Soochow University, Suzhou 215123, People’s Republic of China

3

Department of Psychology, Sun Yat-sen University, Guangzhou 510275, People’s Republic of China

4

School of Psychology, Northeast Normal University, Changchun 130024, People’s Republic of China





spatial IOR toward the farther depth plane was more than a simple effect of attentional orienting. Rather, the inhibitory tagging mechanism may take place. In addition, orienting to the close depth plane resulted in either a facilitatory or null effect. Accordingly, only the pre-response-level conflict was modulated by attentional orienting to the closer depth plane. Keywords  Inhibition of return (IOR) · Flanker effect · Pre-response and response conflicts · Three-dimensional (3D) space

Introduction It has been well documented that there exist three functionally and anatomically independent attention networks in the human brain: the orienting network, the executive network, and the alerting network (Fan et al. 2002, 2003a, b, 2005; Petersen et al. 1989; Posner and Petersen 1990). The orienting network, including areas of dorsal frontoparietal cortex (Corbetta et al. 2000; Fan et al. 2005; Kincade et al. 2005; Yantis et al. 2002), is involved in voluntarily or reflexively shifting attentional focus to a specific location to sample sensory inputs. Moreover, the orienting network is also involved in a spatial inhibitory mechanism that slows down attentional reorienting to the previously attended (cued) location and thus increases the efficiency of visual search (Lepsien and Pollmann 2002; Mayer et al. 2004a, b; Muller and Kleinschmidt 2007; Rosen et al. 1999; Zhou and Chen 2008). This inhibitory mechanism was first revealed in the Posner’s spatial-cuing task. A peripheral cue is first presented to attract spatial attention to the cue location, and if the cue-target stimulus onset asynchrony (SOA) is shorter than 300 ms, then responses to a target

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immediately appearing at the cued location, compared to responses to a target at an uncued location, will be both faster and more accurate. However, if SOA is longer than 300 ms and the cue is not informative with regard to target location, responses to the target at the cued location will be delayed, compared to responses to the target at the uncued location (Klein 2000; Posner and Cohen 1984; Posner et al. 1985). This inhibitory effect is called inhibition of return (IOR). The executive network, including prefrontal regions in the anterior cingulate cortex (ACC) and the dorsal lateral prefrontal cortex (DLPFC) (Botvinick et al. 2001; Fan et al. 2003a, b, 2005), is involved in the various types of executive functions (e.g., the Stroop effect, the flanker effect, and the Simon effect) to resolve conflicts (Botvinick et al. 2001; MacDonald et al. 2000), to suppress inappropriate representations and responses (Gazzaley et al. 2005, 2007), and to implement attentional sets (Dosenbach et al. 2006). Although there has been extensive evidence suggesting the functional and anatomical independence between the executive and the orienting networks, more and more evidence revealed functional interactions between the two attentional networks at both the behavioral and the neural levels (Fuentes 2004; Fuentes et al. 2012). For example, at the behavioral level, Posner and Presti (1987) combined a spatial orienting task and a demanding executive task (counting back from a three-digit number) and found that increasing processing demands in the executive network modulated the functioning of the orienting network. On the other hand, attentional orienting may also affect the resolution of perceptual and response conflicts in the executive network. For example, when the flanker or Stroop interference tasks are combined with the manipulation of IOR such that conflicting information can be presented at either the cued or the uncued location, the interference effects are reduced, eliminated, or even reversed at the cued location (Fuentes et al. 1999; Vivas and Fuentes 2001; Vivas et al. 2007). At the neural level, by combining spatial IOR and the Stroop effect, we found that neural activity in ACC and DLPFC of the executive network was differentially modulated depending on whether the conflicting Stroop information was within or out of the current attentional focus (Chen et al. 2006a, b). Moreover, by combining the spatial IOR which implicated the orienting network and the semantic IOR which implicated the executive network, we found that the orienting and the executive networks complemented each other in biasing the organism toward novel objects: The orienting network was involved in slowing down responses to the old location only when the semantic IOR mechanism in the executive network was not operative; the prefrontal executive network was involved in slowing down responses to the old semantic representation only when the spatial IOR mechanism in the orienting network was not functioning (Chen et al. 2010).

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Although the interaction between visuospatial orienting of attention and executive control has been well established in two-dimensional space, little is known about their interaction in three-dimensional space. Previous evidence suggested that attentional orienting/reorienting in threedimensional world was substantially different from that in two-dimensional world. Previous behavioral studies found that there exist greater costs for shifting attention from near to far locations than for shifting attention from far to near locations, and it was thus proposed that attentional resources are allocated in depth in a viewer-centered fashion, with the maximum processing resources allocated to the stimuli near the observer’s body (Downing and Pinker 1985; De Gonzaga Gawryszewski et al. 1987; Maringelli et al. 2001). Recently, by incorporating the Posner spatial cueing paradigm into a virtual 3D environment in the MR scanner, we investigated the neural mechanisms underlying visuospatial orienting/reorienting along the depth dimension of space. Behaviorally, attentional reorienting to objects unexpectedly appearing closer to the observers in the unattended hemispace was significantly faster than reorienting to unexpected objects farther away. At the neural level, bilateral pre-motor cortex is specifically involved in attentional reorienting in depth (from near to far or vice versa), and the default-mode network is specifically involved in reorienting attention to unattended location in near space (Chen et al. 2012b). Although behavioral and neural mechanisms underlying the early facilitatory orienting component in 3D world have been well documented, it remains poorly understood how visuospatial attention is prevented from returning previously attended location along the depth dimension and how the spatial IOR interacts with executive functions in the 3D world. In the present study, by adopting the spatial cueing paradigm (Posner and Cohen 1984) and constructing a virtual 3D environment, we combined the manipulations of spatial IOR and the flanker interference effect (Fuentes et al. 1999) to investigate the mechanisms underlying the interactions between IOR and the flanker effect in the 3D space. In Experiment 1, we adopted the bilateral flanker paradigm, in which the target was presented at a central location accompanied by bilateral flankers. The flanker display could be presented either at the cued or at the uncued depth plane (Figs. 1a, 2). Since both the target and the bilateral flankers were presented in the same depth plane in Experiment 1, in order to further investigate how the depth of conflicting information influences the interaction between spatial IOR and executive control, we manipulated the spatial location of the flanker in Experiment 2. A unilateral flanker paradigm was used: The unilateral flanker could be presented either at the cued or at the uncued depth plane and could be either close or far from the participants (Figs. 1b, 5).

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Fig. 1  Top view of the experimental setup in Experiments 1 (a) and 2 (b)

Fig. 2  Top view of the various types of exemplary trials in Experiment 1. The default visual scene consisted of six placeholders (three in a closer and three in a farther depth plane) and one fixation cross with equal depth distance between the closer and the farther depth plane

In addition, it has been well documented that attending to space within (near space) and beyond (far space) arm’s reach is subserved by distinct brain circuits (Berti and Frassinetti 2000; Halligan and Marshall 1991; Mennemeier et al. 1992; Previc 1998; Vuilleumier et al. 1998). Because an individual can directly act on and manipulate objects in near space, the dorsal visual stream, which transforms visual information into sensorimotor representations (Goodale and Milner 1992; Goodale et al. 1991; Milner and Goodale 1995), is implicated in near-space processing, and

accordingly, the near space is also termed as the “action space.” By contrast, because no direct actions can be implemented in far space, the ventral stream, which transforms visual information into perceptual representations (Goodale and Milner 1992; Goodale et al. 1991; Milner and Goodale 1995), is involved in the conscious perception of objects in far space, and accordingly, the far space is also termed as the “perception space” (Chen et al. 2012a; Weiss et al. 2003). In order to further investigate how the spatial IOR interacts with the pre-response-level and the response-level

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conflicts in the action (near) and the perception (far) spaces, we differentiated the flanker interference into the per-response and the response levels by using four stimuli (e.g., A, B, 4, 5), with letters (e.g., A, B) requiring one response and digits (e.g., 4, 5) requiring the other response (Chen and Zhou 2013; Chen et al. 2006a, b; Eriksen and Schultz 1979; Milham et al. 2001; Van Veen et al. 2001). Three congruency conditions were manipulated: the congruent (CO) condition, the stimulus incongruent (SI) condition, and the response incongruent (RI) condition. In the congruent (CO) condition, the target and the flanker were identical. In the stimulus incongruent (SI) condition, the target and its flanker were either both letters or both digits and thus required the same response. Therefore, in the SI condition, there existed conflicts only at the pre-response level, but not at the response level. In the response incongruent (RI) condition, the target and its flanker were one letter and one digit (e.g., A and 4) and thus required different responses. Therefore, in the RI condition, there existed conflicts at both the pre-response and the response levels. Relative to the CO condition, the SI condition evoked conflicts only at the pre-response level, and relative to the SI condition, the RI condition evoked conflicts only at the response level.

Experiment 1 Methods Participants Twenty-three (mean age 21.35 ± 1.8 years, 13 females) participants took part in Experiment 1. They were all righthanded and had normal or corrected-to-normal vision and color vision. None of them had a history of neurological or psychiatric disorders. All participants gave their informed consent prior to the experiment in accordance with the Helsinki Declaration and were paid afterward. This study was approved by the Academic Committee of the School of Psychology, South China Normal University, China. Apparatus and stimuli All stimuli were presented on a 27-inch ASUS 3D monitor driven by a Nvidia GeForce FX 5200 graphic card. A pair of Nvidia 3D shutter glasses synchronized with the monitor provided two separated stereoscopic display to each of the two eyes, respectively, with a resolution of 800 (horizontal)  × 600 (vertical) pixels at a refresh rate of 60 Hz. All the 3D objects were presented on a black background by custom-made presentation scripts (Presentation Software package, Neurobehavioral Systems).

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The default virtual display in each trial consisted of three white placeholders in a closer depth plane, another three white placeholders in a farther depth plane, and a central fixation cross between the closer and the farther depth planes (Fig. 2). The 3D objects in the farther depth plane appeared behind the monitor screen, whereas the 3D objects in the closer depth plane popped out of the monitor screen. The central fixation cross was presented on the midsagittal plane of the participant and had an equal depth distance between the closer and the farther depth planes. The binocular disparity between the closer and farther depth planes was ±52.40 min of arc relative to the fusion plane at which the fixation cross was presented (zero disparity). Participants reported that they had a clear perception of the closer and the farther depth planes when fixating at the central fixation cross. The visual angle of the central fixation cross was 0.93°. The horizontal spatial distance (along the x axis) between the left and right placeholders in the closer and the farther depth planes was matched in visual angle (16.85°); i.e., the retinal distance between the spatial positions was matched for the closer and the farther depth planes. The 3D objects in both depth planes were of the same perceived size, resulting in slightly different retinal sizes of the closer and the farther stimuli: 1.98° for the closer and 1.52° for the farther objects. In order to avoid the occlusion between the near and far objects, stimuli in different depth planes were slightly shifted so that the vertical retinal distance between the closer and farther positions was 2.36° of visual angle. For the half of participants, the positions in the closer depth plane were lower and vice versa for the other half of participants. The peripheral cue and the central cue consisted of a transient flash of one of the peripheral (closer or father) placeholders and the central fixation cross, respectively. In addition to the discrimination task, a peripheral detection task was included in which participants were instructed to detect the abrupt appearance of a blue sphere in one of the peripheral locations in the closer or far depth plane. By using the peripheral detection trials, we could test whether the manipulation of visuospatial orienting of attention was effective and whether the IOR phenomenon could be observed in the present 3D environment. In the detection task, the target was a blue sphere; in the discrimination task, the target and the flankers were digits or letters in the black font. Procedure and experimental design At the beginning of each trial, the central location in either the closer or the farther depth plane was cued for 300 ms and was followed by a 200-ms inter-stimulus interval. Subsequently, the spatial location of the central fixation cross was cued for 300 ms to attract attention away from the

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central location in either the closer or farther depth plane. After another period of 150 or 250 ms (to prevent temporal orienting), the target was presented. For the detection task, the target (a blue ball) was presented for 250 ms at the central location of either the cued or the uncued depth plane with equal probabilities, and participants were asked to press the space on the keyboard with their right thumb if they detected the appearance of a blue sphere at the central position in the closer or the farther depth plane. For the discrimination task, the central target together with bilateral flankers was presented for 450 ms either in the closer or in the farther depth plane, with the target being present in the central location and bilateral flankers being presented in the two peripheral locations, and participants were instructed to respond as quickly and as accurately as possible to the target at the central position by pressing one key on the keyboard with their left index finger for the digits and another key on the keyboard with their right index finger for the letters. The stimulus-button mapping was counterbalanced across participants. Participants sat in a dimly lit room and were instructed to fixate at the central fixation cross (zero disparity) throughout the experiment. Before the formal test, each participant performed a practice session in which the composition of different types of trials was the same as that in the formal experiment. Therefore, the experimental design in the discrimination task was a two (depth of target: closer vs. farther) by two (cue validity: cued vs. uncued) by three (flanker congruency: CO, SI, and RI) within-participants design, resulting in twelve experimental conditions in total and 48 trials in each of the experimental conditions. The experimental design in the detection task was a two (depth of target: closer vs. farther) by two (cue validity: cued vs. uncued) within-participants design, resulting in four experimental conditions in total and 48 trials in each of the experimental conditions.

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Results and discussion Incorrect responses and RTs beyond three standard deviations were discarded. Errors in the detection task and the discrimination task were below 3 % across all the conditions and were not further analyzed. Correct RTs in the detection task were entered into a two (depth of target: closer vs. farther) by two (cue validity: cued vs. uncued) repeated-measures ANOVA. The main effect of the depth of target was significant, F (1, 22) = 7.78, p 

Interaction between spatial inhibition of return (IOR) and executive control in three-dimensional space.

It has been well documented how spatial inhibition of return (IOR) interacts with executive functions in a two-dimensional plane, i.e., significantly ...
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