Effect of Spatial Attention on Spatiotopic Visual Motion Perception

Journal of Vision (2019) 19(4):4, 1–19 1

Effect of spatial attention on spatiotopic visual motion perception Graduate School of Integrated Arts and Sciences, # Sanae Yoshimoto Hiroshima University, Hiroshima, Japan $ Department of Psychology, Japan Women’s University, # Tatsuto Takeuchi Kanagawa, Japan $

We almost never experience visual instability, despite objects (Adelson & Bergen, 1985; Anstis, 1980; retinal image instability induced by eye movements. How Braddick, 1980; van Santen & Sperling, 1984; Watson the stability of visual perception is maintained through & Ahumada, 1985). Lower visual areas, such as the spatiotopic representation remains a matter of debate. primary visual cortex (V1), encode input information The discrepancies observed in the findings of existing retinotopically (e.g., Wandell, Brewer, & Dougherty, neuroscience studies regarding spatiotopic representation 2005). Retinal images change in a complex manner partly originate from differences in regard to how attention is deployed to stimuli. In this study, we because of eye, head, or body movements. Because we psychophysically examined whether spatial attention is perceive the visual world as stable and detect object needed to perceive spatiotopic visual motion. For this motion veridically from complex retinal images, there purpose, we used visual motion priming, which is a must be a mechanism that constructs nonretinotopic phenomenon in which a preceding priming stimulus representation in the visual pathway. How the stability modulates the perceived moving direction of an of visual perception is maintained has a long history of ambiguous test stimulus, such as a drifting grating that study and remains a matter of debate (Burr & phase shifts by 1808. To examine the priming effect in Morrone, 2012; Cavanagh, Hunt, Afraz, & Rolfs, 2010; different coordinates, participants performed a saccade Marino & Mazer, 2016; Melcher & Morrone, 2015; soon after the offset of a primer. The participants were Wurtz, 2008). A promising mechanism of visual tasked with judging the direction of a subsequently stability was proposed by Helmholtz (1867), which was presented test stimulus. To control the effect of spatial attention, the participants were asked to conduct a based on a copy of saccade motor command, termed concurrent dot contrast-change detection task after the efference copy, or corollary discharge (e.g., Duhamel, saccade. Positive priming was prominent in spatiotopic Colby, & Goldberg, 1992; Sommer & Wurtz, 2002; conditions, whereas negative priming was dominant in Wurtz, 2008). An efference copy, also called a corollary retinotopic conditions. At least a 600-ms interval between discharge, is a copy of a motor command sent to brain the priming and test stimuli was needed to observe areas for interpreting sensory inﬂow. Theoretically, an positive priming in spatiotopic coordinates. When spatial efference copy signal could update the incoming visual attention was directed away from the location of the test signal to create a gaze-invariant spatiotopic represen- stimulus, spatiotopic positive motion priming completely tation from the retinotopic visual input; however, disappeared; meanwhile, the spatiotopic positive motion whether spatiotopic representation is actually a key priming at shorter interstimulus intervals was enhanced factor in solving the problem of visual stability is also a when spatial attention was directed to the location of the matter of debate (Burr & Morrone, 2012; Zimmer- test stimulus. These results provide evidence that an attentional resource is requisite for developing spatiotopic mann, Morrone, & Burr, 2014). In line with this representation more quickly. discussion, the question of which reference frame, such as a retinotopic reference frame or a spatiotopic (or world-centered) reference frame, visual motion perception depends on is fundamental in the ﬁeld of Introduction research of visual stability regarding visual motion perception (e.g., d’Avossa et al., 2007; Knapen, Rolfs, The human visual system contains specialized & Cavanagh, 2009; Turi & Burr, 2012; Wenderoth & mechanisms for analyzing the velocity of moving Wiese, 2008).

Citation: Yoshimoto, S., & Takeuchi, T. (2019). Effect of spatial attention on spatiotopic visual motion perception. Journal of Vision, 19(4):4, 1–19, https://doi.org/10.1167/19.4.4.

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To examine whether spatiotopic information is Yoshimoto, Uchida-Ota, & Takeuchi, 2014a; Yoshi- explicitly represented or encoded in the visual motion moto, Uchida-Ota, & Takeuchi, 2014b; see summary system, d’Avossa et al. (2007) measured functional by Marino & Mazer, 2016, table 3). In this study, magnetic resonance imaging (fMRI) responses while consequently, we used the visual motion priming presenting visual motion stimuli and manipulating gaze paradigm (Ong et al., 2009; Yoshimoto et al., 2014a; direction. They consequently found spatiotopic re- Yoshimoto et al., 2014b) in addition to concurrently sponses in the human middle temporal (MT) area, conducting a dot contrast-change detection task which indicated spatial selectivity based on screen (Crespi et al., 2011) to control the spatial attention of coordinate rather than retinotopic coordinate for visual spatiotopic motion perception. motion perception. On the other hand, Gardner, Visual motion priming is a phenomenon in which the Merriam, Movshon, and Heeger (2008), using a similar preceding moving stimulus (primer) modulates the motion task, found no evidence of spatiotopic fMRI perceived direction of a directionally ambiguous test responses in the visual cortex and concluded that all stimulus (Anstis & Ramachandran, 1987; Campana, representations in the visual cortex are retinotopic. Pavan, & Casco, 2008; Heller & Davidenko, 2018; Crespi et al. (2011) examined the discrepancy between Jiang, Luo, & Parasuraman, 2002; Jiang, Pantle, & these two studies by manipulating spatial attention, Mark, 1998; Kanai & Verstraten, 2005; Pantle, because the participants in d’Avossa et al. (2007) paid Gallogly, & Piehler, 2000; Pavan, Campana, Guerre- attention to peripherally presented motion stimuli, schi, Manassi, & Casco, 2009; Piehler & Pantle, 2001; whereas those in Gardner et al. (2008) attended to the Pinkus & Pantle, 1997; Ramachandran & Anstis, 1983; center of the display while motion stimuli were Raymond, O’Donnell, & Tipper, 1998; Takeuchi, presented at the periphery. By conducting a peripher- Tuladhar & Yoshimoto, 2011; Yoshimoto & Takeuchi, ally presented motion discrimination task, Crespi et al. 2013). In negative motion priming, the test stimulus is (2011) found spatiotopic responses in area MT or perceived to move in the opposite direction to the middle superior temporal (MST) in the free-viewing priming stimulus. Meanwhile, in positive motion, conditions, in which attention was not controlled. priming the test stimulus is perceived to move in the However, when the participants performed a dual task, same direction as that of the priming stimulus. As in which their attention was conﬁned to the fovea, only described in the Methods section of Experiment 1, retinotopic responses were observed in the visual whether positive or negative priming occurs depends on cortex. These ﬁndings of Crespi et al. (2011) indicate a range of factors, such as the presentation duration, the necessity, for the spatiotopic fMRI response, of luminance contrast, and velocity of the priming attending to motion stimuli or the location where the stimulus used (Pinkus & Pantle, 1997; Kanai & motion stimuli will appear. As highlighted by Melcher Verstraten, 2005; Takeuchi et al., 2011; Yoshimoto & and Morrone (2015, p. 7), however, it is not certain Takeuchi, 2013). whether the participants actually directed their atten- In our previous studies (Yoshimoto et al., 2014a; tion to the peripherally presented motion stimuli in the Yoshimoto et al., 2014b), participants performed free-viewing conditions of Crespi et al. (2011). saccades after the offset of a drifting sine-wave priming In this study, therefore, we directly manipulated stimulus and judged the direction of a directionally spatial attention to psychophysically examine whether ambiguous test stimulus that was displayed in retino- spatial attention is needed for spatiotopic visual motion topic or spatiotopic coordinates. Through these exam- perception. A standard way of examining the spatio- inations, we found that positive motion priming is topic effect is to present an observer with two stimuli spatiotopic whereas negative priming is predominantly over time in the same spatial (screen-based) position, retinotopic. Thus, positive priming was never perceived separated by a saccade that causes the two stimuli to when the spatial locations of the priming and test fall in different retinal locations (Melcher, 2005; stimuli were retinotopically coincident before and after Melcher & Colby, 2008; Melcher & Morrone, 2015). the saccade; on the other hand, negative motion Preparing two moving stimuli and examining whether priming did not occur when the spatial locations of the these moving stimuli interact through adaptation or priming and test stimuli were coincident. priming would help us to understand the characteristics By using these characteristics of visual motion of spatiotopic effects on visual motion perception priming, such that spatiotopic positive motion priming (Biber & Ilg, 2011; Burr, Cicchini, Arrighi, & Morrone, and retinotopic negative motion priming can be 2011; Burr, Tozzi, & Morrone, 2007; Ezzati, Golzar, & exclusively observed, we examined whether manipula- Afraz, 2008; Fracasso, Caramazza, & Melcher, 2010; tion of spatial attention affects spatiotopic and/or Knapen et al., 2009; Melcher & Fracasso, 2012; retinotopic motion perception. If spatial attention is Melcher & Morrone, 2003; Ong, Hooshvar, Zhang, & requisite for inducing spatiotopic motion perception, as Bisley, 2009; Seidel Malkinson, Mckyton, & Zohary, predicted from the aforementioned fMRI studies 2012; Turi & Burr, 2012; Wenderoth & Wiese, 2008; (Crespi et al., 2011; d’Avossa et al., 2007; Gardner et

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al., 2008), it is expected that positive motion priming is larly. We monitored the movements of each partici- not perceived if participants’ attention is directed away pant’s right eye using an infrared video–based eye- from the future location of the test stimulus. To control tracking device (ViewPoint EyeTracker 220 fps USB spatial attention, we conducted a dot contrast-change system, Arrington Research, Inc., Scottsdale, AZ) with detection task similar to that used in Crespi et al. (2011) a 220-Hz sampling rate. The eye tracker was controlled as a secondary task. by ViewPoint software version 2.9.5.137 (Arrington Research, Inc.).

Experiment 1 Visual stimulus Figure 1 shows the stimulus configuration of a trial Methods in Experiment 1. This configuration was similar to that used in our previous studies (Yoshimoto et al., 2014a; Participants Yoshimoto et al., 2014b) in order to allow comparison Twenty-six individuals (11 men and 15 women; with the present results. An achromatic vertical sine- average age ¼ 21.6 years, range 19–27 years) with wave grating (spatial frequency ¼ 0.5 cycles per degree normal or corrected vision participated in Experiment in visual angle [c/8]) was displayed in a rectangular 1; all were undergraduate and graduate students from window (10.08 w 3 3.38 h). The edges of the stimulus Hiroshima University who volunteered to participate in were tapered using a Gaussian function (r ¼ 1.08). The this study and were na¨ıve to the purpose of the stimuli were presented on a uniform gray-colored experiment. The study followed protocols approved by background with a luminance identical to the space- the Institutional Research Boards of Hiroshima Uni- averaged luminance of the stimuli. versity and was conducted in accordance with the Various stimulus parameters have been shown to Declaration of Helsinki. All participants provided influence the perception of visual motion priming written informed consent before engaging in the study. (Kanai & Verstraten, 2005; Pantle et al., 2000; Pavan & Two participants were excluded because their perfor- Skujevskis, 2013; Pinkus & Pantle, 1997; Takeuchi et mance in the attentional task was too low, as described al., 2011; Yoshimoto & Takeuchi, 2013). Yoshimoto below; thus, the reported results were derived from 24 and Takeuchi (2013) found that the velocity and participants (10 men and 14 women; average age ¼ 21.7 duration of the primer determined motion priming years, range 19–27 years). effects when the stimuli presented in the parafovea had a high luminance contrast (higher than 10 times the direction discrimination threshold). At a velocity of 3 Apparatus Hz, positive priming was observed when the primer The stimuli were generated using MATLAB R2017b duration was shorter than 300 ms; in contrast, when the (MathWorks, Natick, MA) and the Psychophysics primer duration was longer, negative motion priming Toolbox Version 3 (PTB-3; Brainard, 1997; Pelli, 1997) was observed. However, at velocities lower than 3 Hz, on a PC (Applied WST-E52609V4S3Q1TT worksta- positive priming was prominent even when the primer tion, Applied Co., Ltd., Fukuoka, Japan). These were duration was as high as 2,000 ms. At velocities higher then displayed on a 27-in. flat screen liquid crystal than 3 Hz, negative priming was observed regardless of display (LCD) monitor (EIZO FORIS FS2735, EIZO primer duration. These results indicate that the specific Co., Ishikawa, Japan). This high-end gaming monitor priming effect (negative or positive) is robustly induced is a successor model to the EIZO FG2421, which was by properly manipulating the velocity and duration of recommended as a replacement for a cathode ray tube the priming stimulus. (CRT) when running visual psychophysics (Ghodrati, In this study, we examined the effect of certain Morris, & Price, 2015). The monitor had an 8-bit gray- combinations of primer duration and velocity in terms level spatial resolution of 2,560 3 1,440 pixels with a of inducing positive or negative priming. The duration frame rate of 120 Hz, and its output was gamma- of the primer was set to 167 or 1,000 ms and its velocity corrected by a ColorCAL MKII colorimeter (Cam- was set to 2, 3, or 4 Hz. To equate the velocity of the bridge Research Systems Ltd., Rochester, UK). The test stimulus to that of the primer, the duration of one average luminance of the screen was set to 72.4 cd/m2. frame of the test stimulus was set to be equal to the The room was darkened and shielded from light, with duration required for the primer to shift 1808. The test no other source of illumination present. Participants stimulus had a total of four frames. The luminance observed the display while maintaining their heads in a contrast determined by the Michaelson relationship of consistent position, which was achieved using a chin the priming and test stimuli was 50%. and head rest. The viewing distance was set to 57 cm, The priming stimulus was displayed in the center of and the participants viewed the visual stimuli binocu- the screen. The spatial distance between the center of

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Figure 1. Stimulus configuration of a trial in Experiment 1. A fixation dot (depicted in red here for the purpose of illustration, but it was actually dark gray in the experiment) was displayed to help participants to maintain fixation. Under the retinotopic (A) and spatiotopic (B) conditions, participants performed a saccade when the fixation dot jumped to a new location after the offset of the primer. After a variable ISI, the test stimulus was displayed above (A) or below (B) the new fixation dot. Under the full (C) and unmatched (D) conditions, the position of the fixation dot was not changed; thus, saccades were not required. After the ISI, the test stimulus was displayed above (C) or below (D) the fixation dot. Three conditions were examined to control spatial attention. In the !

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condition with no attentional task (‘‘w/o task’’), only the fixation dot was presented. In the ‘‘Identical’’ and ‘‘Different’’ conditions, another dark-gray dot was presented during a variable ISI, either in the same (‘‘Identical’’) or opposite (‘‘Different’’) side of the test stimulus. The dot contrast was increased or decreased at some points during the ISI after the saccade. In this figure, only the condition when the dot contrast increased is presented.

the gratings and the fixation dot was set to 3.38. A dark- spatiotopic nor retinotopic location of the primer, with gray dot with a luminance of 57.9 cd/m2 and a diameter no shift in the fixation dot (Figure 1D). The unmatched of 0.58 was displayed to help participants maintain condition was used to examine the possibility that the fixation during trials. Similar to our previous studies effects of motion priming could result from motion (Yoshimoto et al., 2014a; Yoshimoto et al., 2014b), we integration over a large spatial region in the spatiotopic measured the priming effect at four frame of reference condition when the priming and test stimuli were conditions (Figure 1). In the retinotopic condition, a separated retinotopically. dark-gray–colored fixation dot (depicted as a red pot in To confirm whether the priming effect is robust to Figure 1) shifted to the upper region of the screen the retinal location, four individuals who were not immediately after the termination of the primer, and involved in Experiment 1 performed the motion the test stimulus was presented in the same retinotopic priming task not only when the primer was presented in location as the primer relative to fixation after a the upper peripheral retina (above the fixation dot) but variable interstimulus interval (ISI; Figure 1A). In the also when the primer was presented in the lower spatiotopic condition, the fixation dot was shifted as in peripheral retina (below the fixation dot), prior to the the retinotopic condition, but the test stimulus was actual data acquisition. The spatial location of the test presented in the same screen location as the primer stimulus was determined based on the frame of (Figure 1B). In the full condition, the test stimulus was reference condition (retinotopic, spatiotopic, full,or presented in the same location as the primer after a unmatched). Consequently, no systematic difference in variable ISI. Because the fixation dot was not shifted, the priming effect was found between upper and lower this condition represented both retinotopic and spa- peripheral retina. Therefore, in the actual experiment, tiotopic coordinates (Figure 1C). In the unmatched the primer was presented only in the upper peripheral condition, the test stimulus was presented after a retina (Figure 1). Participants made 6.78 upward variable ISI in a position that matched neither the saccades with the shift of the fixation dot under the retinotopic and spatiotopic conditions (Figures 1A and Primer 1B) but not under the full and unmatched conditions duration Velocity Predicted priming effects (Figures 1C and 1D). (ms) (Hz) with no attentional task The combinations of the durations and velocities of the primer in Experiment 1 are shown in Table 1. We 167 3 Positive under the spatiotopic and full examined combinations of the duration and velocity of conditions the primer because manipulating a single parameter is No priming under the retinotopic and not sufficient to determine the priming effect. Predic- unmatched conditions tions regarding the perceived direction of the test 167 4 Negative under the retinotopic and full stimulus were also included; they were based on a conditions previous study that demonstrated the effects of the No priming under the spatiotopic and durations and velocities of priming stimuli in various unmatched conditions coordinate frames (Yoshimoto et al., 2014b). No effect 1,000 2 Positive under the spatiotopic and full of spatial attention has been taken into account in conditions Table 1. No priming under the retinotopic and Previous studies have shown that spatiotopic per- unmatched conditions ception is not available instantaneously. Spatiotopicity 1,000 3 Negative under the retinotopic and full requires 500–1,000 ms to develop, depending on the conditions experimental situation. A delay between saccade No priming under the spatiotopic and initiation and test presentation or a delayed period unmatched conditions between saccade end and test presentation has been Table 1. The stimulus parameters examined in Experiment 1 shown to be necessary for spatiotopic representation coupled with the predicted priming effects with saccade, which (Burr & Morrone, 2011; Burr & Morrone, 2012; were based on the findings of Yoshimoto et al. (2014b). Notes: Golomb, Nguyen-Phuc, Mazer, McCarthy, & Chun, These predictions do not take the effect of spatial attention into 2010; Golomb, Marino, Chun, & Mazer, 2011; account. Golomb, Pulido, Albrecht, Chun, & Mazer, 2010;

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Mathoˆt & Theeuwes, 2010; Morrone, Cicchini, & Burr, the screen after the offset of the primer. Participants 2010; Zimmermann, Morrone, & Burr, 2014; Zimmer- were required to make a saccade to the new location of mann, Morrone, Fink, & Burr, 2013). Yoshimoto et al. the fixation dot and were instructed to maintain their (2014a, 2014b) showed that positive priming in gaze on the fixation dot throughout the trial. The task spatiotopic conditions was observed only when the was to report the perceived direction (rightward or interval between the priming and test stimuli was longer leftward) of the test stimulus. Participants pressed the than 400 ms. Therefore, as in Yoshimoto et al. (2014b), corresponding arrow key on the computer keyboard to the ISI between the offset of the primer and onset of the report their judgment. In the ‘‘Identical’’ and ‘‘Different’’ test stimulus was changed from 400 to 3,000 ms for this attentional conditions, another dot was presented either experiment. The ISI was also changed in the full and above or below the fixation dot during an ISI period. unmatched conditions in the same manner as for the The contrast of this dot was changed at some point retinotopic and spatiotopic conditions. during the ISI. In the condition with no attentional task For each of the four conditions of the different (the ‘‘w/o task’’), only the fixation dot was presented reference frames shown in Figure 1, three task during the ISI. After the ISI, a test stimulus was conditions for controlling spatial attention were ex- presented. In the two attentional conditions (‘‘Identical’’ amined. In the ‘‘w/o task’’ condition, no concurrent and ‘‘Different’’), after the direction judgment, the attentional task was conducted. Meanwhile, in the participants also reported whether they perceived the dot ‘‘Identical’’ and ‘‘Different’’ conditions shown in Figure contrast to have increased or decreased compared with 1, participants were required to perform dot contrast- the original contrast by pressing the 1 key (increased) or change detection judgment (attentional task) in addi- 2 key (decreased) on the keyboard. After they made a tion to motion direction judgment (priming task). In selection, a 1-s intertrial interval (in which a uniform these two conditions, a dark-gray dot (red-colored dot field with space-averaged luminance was displayed) was in Figure 1) continued to appear 3.38 above or below inserted to reduce the effect of the former trial. Each the fixation dot during the ISI between the primer and session consisted of 64 trials: four trials for each of the test stimulus; the luminance and the diameter of this eight ISIs between the primer and test stimulus (400, dot were the same as those of the fixation dot. In the 600, 800, 1,000, 1,200, 1,600, 2,000, and 3,000 ms), and ‘‘Identical’’ condition, the position of the dot was for the two directions of the primer (leftward or identical to that of the center of the test stimuli, whereas in the ‘‘Different’’ condition, the position of rightward), which were presented in a random order. In the dot was vertically opposite to the side of the test each session, the duration of the priming stimulus, the stimuli. The dot contrast was increased or decreased by velocity, and the coordinate conditions were fixed. The 30% at a random time during the ISI, and the contrast four parameter combinations show in Table 1 were change lasted 50 ms (depicted as a light-gray–colored examined at each of the four coordinate conditions. dot in Figure 1). To avoid a saccadic inhibition in the When the participants performed the motion direction retinotopic and spatiotopic conditions, the dot contrast judgment as well as the dot contrast judgment, the dot was changed at least 300 ms after the fixation dot position (‘‘Identical’’ or ‘‘Different’’ condition) was also shifted. Therefore, as shown in Figures 1A and 1B, in fixed in each session. Each participant completed four both the ‘‘Identical’’ and ‘‘Different’’ conditions, the ISI sessions for each of the four parameter combinations at was divided into the ‘‘saccade’’ period (continues for each of the four reference frame conditions and at each 300 ms) and the ‘‘attentional task’’ period (varying of the three attentional task conditions in random order. from 100 to 2,700 ms in duration, depending on the Each session took approximately 10 min to complete. total length of the ISI). This procedure was also Each participant completed a total of 192 sessions in 3 adopted in the full and unmatched conditions, in which months. Participants underwent at least 20 practice trials no saccade was required. These parameters of dot under each condition prior to data acquisition. presentation were adjusted to maintain the partici- During the experiment, eye movement was moni- pants’ rate of correct answers at approximately 95%, tored using the infrared video–based eye-tracking which is the same criterion as that used by Crespi et al. system described above. All eye movement analysis was (2011). conducted offline. Prior to the saccade detection, eye blinks were removed by the ViewPoint software (Arrington Research, Inc.) from the eye recording data. Procedure Saccade onset and offset were detected by applying a Each trial began with the presentation of a fixation set of velocity and acceleration criteria, using 408/s dot for 1.5 s. The primer subsequently appeared while velocity and 8008/s2 acceleration thresholds (Krauzlis & the fixation dot was continuously presented on the Miles, 1996), by the combination of ViewPoint screen. In the retinotopic and spatiotopic conditions, the software and in-house software implemented by fixation dot immediately shifted to the upper region of MATLAB.

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Figure 2. Averaged data for the participants in Experiment 1. In each graph (retinotopic, spatiotopic, full, and unmatched conditions), the percentage positive priming responses (perceiving the test stimulus to have moved in the same direction as that of the primer) is plotted as a function of the ISI between the priming and test stimuli (in milliseconds). Each curve represents data that were collected in the attentional conditions (‘‘Identical’’ or ‘‘Different’’ conditions) and in the condition with no attentional task (‘‘w/o task’’). Error bars represent 95% confidence intervals (CIs). Asterisks indicate significant differences in positive priming between ‘‘w/o task’’ and ‘‘Identical’’ conditions. The primer duration and velocity were set to (A) 167 ms and 3 Hz and (B) 1,000 ms and 2 Hz, respectively.

Results (average of 94.3% correct responses). However, two participants scored well below 90% in regard to correct Fixation and saccades responses (62% and 55%), so we excluded their data We checked whether participants executed saccades from subsequent analyses. in accordance with the shifts of the fixation dot (the red dot in Figure 1). For all trials in the retinotopic and spatiotopic conditions, the duration between the Motion direction judgment termination of the primer and end of the saccade Conditions in which positive priming was predicted: ranged from 132 to 283 ms. Therefore, it can be Figure 2 shows the group-averaged results for each concluded that the ISI of 400 ms was sufficiently long condition. In Figure 2A, the primer duration is 167 ms to perform a 6.78 saccade. In 6.9% of the trials, and the velocity is 3 Hz; in Figure 2B, these values are participants looked more than 1.58 away from the 1,000 ms and 2 Hz, respectively. As shown in Table 1, fixation dot in a single trial at both pre- and positive priming was expected to appear in these postsaccade. We did not conduct subsequent analyses conditions. The percentage response to positive prim- for those trials. ing was plotted as a function of the ISI between the primer and test stimulus. In most of the trials, the participants reported that the perceived direction of the Dot contrast-change detection judgment test stimulus was the same as that of the primer when For the ‘‘Identical’’ and ‘‘Different’’ attentional the percentage response was higher than 50%. On the conditions, in most of the trials, the participants other hand, when the percentage response was lower correctly judged whether the dot contrast had de- than 50%, the participants reported in most of the trials creased or increased relative to that of the original dot that the perceived direction of the test stimulus was in

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the direction opposite to that of the primer (negative the attentional task and ISI was also significant (F(14, 2 priming). 322) ¼ 31.69, p , 0.0001, g G ¼ 0.36. Further, the Positive priming was prominent in the spatiotopic Tukey’s test revealed significant differences in the condition; meanwhile, no priming effect was observed positive priming between ‘‘w/o task’’ and ‘‘Identical’’ in the retinotopic condition when attentional task was conditions at four ISIs (400, 600, 800 and 1,000 ms; qs not required (‘‘w/o task’’). These results fitted our 5.68, ps , 0.001, marked by asterisks in Figure 2B. predictions described in the ‘‘167 ms/3 Hz’’ and ‘‘1,000 In the full condition shown in Figure 2, positive ms/2 Hz’’ conditions in Table 1, which are based on our priming was observed in the condition with no previous studies (Yoshimoto et al., 2014a; Yoshimoto attentional task (‘‘w/o task’’), as predicted in our et al., 2014b). The arch-shaped curve in the spatiotopic previous studies (Yoshimoto et al., 2014a; Yoshimoto ‘‘w/o task’’ condition represents that positive priming et al., 2014b; Table 1). The clear difference here in became prominent in the middle range of the ISI relation to the results of the spatiotopic condition is that (approximately 800–1,600 ms), thus replicating the positive priming was also conspicuous at both atten- results in our previous studies (Yoshimoto et al., 2014a; tional (‘‘Identical’’ and ‘‘Different’’) conditions. In all Yoshimoto et al., 2014b). However, in the attentional of the conditions, the strength of positive priming was condition in the spatiotopic condition, where the dot prominent when ISI was as short as 400 ms but was target appeared in the same position as the test stimuli reduced as ISI became longer. Thus, no effect of (‘‘Identical’’ condition), positive priming was observed attentional manipulation was observed in the full in more than 80% of the trials, even with ISIs as short condition. as 400–600 ms. Meanwhile, no motion priming was In the retinotopic and unmatched conditions, no observed for any ISIs when the dot target appeared in a priming effect was observed in the ‘‘w/o task’’ different location to that of the test stimuli (‘‘Different’’ condition, which also accorded with our prediction condition), regardless of the primer duration and (Table 1). Attentional manipulation had no effect for velocity used. both conditions. To test whether the attentional task altered the Conditions in which negative priming was predicted: positive priming in the spatiotopic condition, which was Figure 3 shows the group-averaged results for each our main interest in Experiment 1, a two-way analysis coordinate condition. In Figure 3A, the duration of the of variance (ANOVA) for repeated measures with priming stimulus is 167 ms and the velocity is 4 Hz; in Tukey’s post hoc test was conducted. Angular trans- Figure 3B, the values are 1,000 ms and 3 Hz, formation was applied for the percentage values to normalize the binomial distribution (Fernandez, 1992); respectively (the predictions for these parameters are thereafter, the homogeneity of variance for the shown in Table 1). For both sets of parameters, for the transformed data sets was confirmed by Bartlett’s test no attentional task (‘‘w/o task’’), negative motion before using the ANOVA. Effect sizes were reported as priming was dominant in both the retinotopic and full 2 conditions, whereas no priming effect was observed in generalized eta-squared (g G), as recommended for repeated-measures designs (Bakeman, 2005; Olejnik & the spatiotopic and unmatched conditions, as predicted Algina, 2003): 0.02 for a small effect, 0.13 for a medium (Table 1). Negative priming was also observed in both effect, and 0.26 for a large effect according to Cohen’s the ‘‘Identical’’ and ‘‘Different’’ attentional conditions. recommendation (Cohen, 1988). At a primer duration The strength of negative priming was prominent when of 167 ms and velocity of 3 Hz in the spatiotopic ISI was as short as 400 ms and was reduced as ISI condition (Figure 2A), the main effects of the became longer and converged to 50%. A two-way attentional task and ISI were significant, F(2, 46) ¼ ANOVA showed that at a primer duration of 167 ms 2 and a velocity of 4 Hz (Figure 3A), the main effect of 384.0, p , 0.0001, g G ¼ 0.71, for the attentional task 2 F and F(7, 161) ¼ 35.02, p , 0.0001, g G ¼ 0.31 for the the attentional task was not significant, (2, 46) ¼ 0.01, ISI; the interaction between the attentional task and ISI ns, whereas that of the ISI was significant, F(7, 161) ¼ 2 2 was also significant, F(14, 322) ¼ 21.51, p , 0.0001, g G 184.9, p , 0.0001, g G ¼ 0.56. The interaction between ¼ 0.26. The Tukey’s test revealed significant differences the attentional task and the ISI was not significant, in the positive priming between ‘‘w/o task’’ and F(14, 322) ¼ 0.73, ns. At a primer duration of 1,000 ms ‘‘Identical’’ conditions at four ISIs (400, 600, 800, and and a velocity of 3 Hz (Figure 3B), the main effect of 1,000 ms; qs 4.00, ps , 0.05), marked by asterisks in the attentional task was not significant, F(2, 46) ¼ 0.07, Figure 2A. At a primer duration of 1,000 ms and a ns, whereas that of the ISI was significant, F(7, 161) ¼ 2 velocity of 2 Hz in the spatiotopic condition (Figure 172.4, p , 0.0001, g G ¼ 0.70. Meanwhile, the 2B), the main effects of the attentional task and ISI interaction between the attentional task and ISI was 2 were significant, F(2, 46) ¼ 390.0, p , 0.0001, g G ¼ not significant, F(14, 322) ¼ 0.94, ns. Thus, it is 0.76, for the attentional task and F(7, 161) ¼ 59.75, p , concluded that no effect of attentional manipulation 2 0.0001, g G ¼ 0.41, for the ISI; the interaction between was observed in the retinotopic and full conditions.

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Figure 3. Averaged data for the participants in Experiment 1. In each graph (retinotopic, spatiotopic, full, and unmatched conditions), the percentage response of positive priming is plotted as a function of the ISI between the primer and test stimulus (in milliseconds). Each curve represents the data that were collected in the attentional conditions (‘‘Identical’’ and ‘‘Different’’ conditions) and in the condition with no attentional task (‘‘w/o task’’). Error bars represent 95% CIs. The primer duration and velocity were set to (A) 167 ms and 4 Hz and (B) 1,000 ms and 3 Hz, respectively.

In accordance with our prediction (Table 1), no right of the Figures 2A and B). In the ‘‘Identical’’ priming effect was observed in the ‘‘w/o task’’ in the condition, the positive priming became prominent spatiotopic and unmatched conditions. Furthermore, at the short ISIs, where none or less positive attentional manipulation had no effect on the percep- priming was observed in the ‘‘w/o task’’ condition. tion of visual motion priming. The priming effect completely disappeared in the ‘‘Different’’ condition. No effect of attentional task was found when the negative priming was Summary of the results observed (Figure 3). Following is a summary of the main ﬁndings of Experiment 1: 1. In the condition with no attentional task (‘‘w/o Discussion task’’), positive priming was observed in the spatiotopic and full conditions but not in the The results obtained in the ‘‘w/o task’’ conditions are retinotopic and unmatched conditions (Figure 2). consistent with our previous results (Yoshimoto et al., Meanwhile, negative priming was observed in the 2014a; Yoshimoto et al., 2014b), even though there are retinotopic and full conditions but not in the several differences between this and the previous spatiotopic and unmatched conditions (Figure 3). experiments, such as the number of participants (four These results are a replication of our previous vs. 24) and the monitor used (CRT vs. LCD). Thus, studies’ results (Yoshimoto et al., 2014a; Yoshi- when a saccade after the offset of the primer was moto et al., 2014b). required, positive priming was observed for the 2. The attentional task only modulated the positive spatiotopic condition, whereas negative priming was priming effect in the spatiotopic condition (upper observed for the retinotopic condition. Pronounced

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positive priming in the spatiotopic condition was with normal or corrected-to-normal vision participated observed only when the ISI was longer than 600 ms. in Experiment 2; all had participated in Experiment 1 Because no priming was observed in the unmatched previously. To test whether the task experience of condition, it can be surmised that the positive priming Experiment 1 influenced participants’ performance in observed in the spatiotopic condition was not the by- Experiment 2, the remaining 20 individuals (eight men product of the spatiotemporal summation of motion and 12 women; average age ¼ 20.7 years, range 19–24 information over a larger area. years) with normal or corrected-to-normal vision were Tests of the effect of spatial attention, controlled by also recruited from Hiroshima University to participate the concurrent dot contrast-change detection task, only in Experiment 2. These participants who were revealed that only the perception of positive priming in undergraduate and graduate students were new ob- spatiotopic reference frames depended on the attended servers and na¨ıve to the purpose of the experiment. One location (Figures 2A and 2B). When spatial attention participant was excluded because of his low perfor- was explicitly directed to the location where the test mance on the attentional task. The reported results stimulus would be presented (‘‘Identical’’ condition), were thereby derived from 19 participants for the the positive priming became conspicuous at shorter second group (seven men and 12 women; average age ¼ ISIs compared with that obtained in the no attentional 20.8 years, range 19–24 years). task (‘‘w/o task’’) condition. However, when spatial attention was directed away from the test stimulus location, in the ‘‘Different’’ condition, the spatiotopic Stimuli positive priming completely disappeared. In the other Figure 4 shows a schematic description of the stimuli reference frame conditions, such an effect of spatial used in one of the trials from Experiment 2. As in attention was not observed at all. These results suggest Experiment 1, we examined the manner in which a that attributing spatial attention to the location where priming stimulus modulated the perceived direction of the stimulus will appear is an important factor for a directionally ambiguous test stimulus. The stimulus perceiving spatiotopic visual motion. However, before configuration was similar to that in the full condition in drawing this conclusion, we conducted another exper- Experiment 1 (Figure 1C), with the exception that the iment (Experiment 2) to examine the effect of saccade fixation dot shifted; specifically, the fixation dot shifted per se on spatiotopic perception. 6.78 to the upper region of the screen immediately after the offset of the priming stimulus, remained there for 200 ms, and then returned to its original position Experiment 2 (Figure 4). Thus, the participants performed two saccadic eye movements to track the fixation dot. We did not expect the saccades to be completed within 200 In Experiment 1, the perception of positive priming ms. This duration was arbitrarily determined to assist was modulated by spatial attention in the spatiotopic condition but not in the full condition (Figures 2A and the participants when performing the saccadic eye B). One obvious difference between these two condi- movements. The ISIs between the offset of the primer tions is the presence of saccades. If saccadic eye and onset of the test stimulus were the same as those movements per se caused the effect of spatial attention used in Experiment 1; however, our previous studies, in in the spatiotopic condition, priming effects would also addition to the preliminary observations in this study, be affected by manipulating spatial attention in the full showed that an ISI of 400 ms is not sufficiently long for condition when participants performed saccadic eye participants to perform two saccades. Therefore, we movements. We examined this possibility in Experi- examined a range of ISIs, from 600 to 3,000 ms. ment 2. Such a control experiment for examining the In the attentional condition, another small dark-gray effect of eye movements per se has been recommended dot was presented 3.38 above (‘‘Identical’’ condition) or for experiments of spatiotopic visual perception below (‘‘Different’’ condition) the initial fixation point (Knapen et al., 2009; Knapen, Rolfs, Wexler, & during the ISIs. The dot contrast was increased or Cavanagh, 2010; Marino & Mazer, 2016; Nieman, decreased by 30%. To avoid an effect of saccadic Hayashi, Andersen, & Shimojo, 2005). inhibition, the dot contrast was changed at least 300 ms after the fixation dot had returned to the initial fixation point. In the ‘‘w/o task’’ condition, dot contrast-change Methods detection was not required. To induce positive priming, the primer duration and velocity were set to 167 ms and Participants 3 Hz or 1,000 ms and 2 Hz, respectively (Table 1; We conducted the experiment with two different Figure 2). The luminance contrast of the stimuli was groups of participants. First, 21 individuals (8 men and 50%. We did not examine the conditions in which 13 women; average age ¼ 21.4 years, range 19–25 years) negative priming would be expected, such as in 167-ms

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Figure 4. Stimulus configuration of a trial in Experiment 2. A dark-gray dot (depicted in red here for the purpose of illustration) was displayed to help the participants maintain fixation. The fixation dot shifted to the upper region of the screen after the offset of the primer, remained there for 200 ms, and then returned to its original position. Thus, the participants performed two saccades to track the fixation dot. In the condition with no attentional task (‘‘w/o task’’), only the fixation dot was presented during the ISIs. After each variable ISI, the test stimulus was presented in the same screen location as the primer. In the attentional conditions, another small dark-gray dot was presented either in the location corresponding to the center of the test stimulus (‘‘Identical’’) or in the location corresponding to the vertically opposite side of the test stimulus (‘‘Different’’) during each ISI. The dot contrast was increased or decreased at a random timing during the ISI but at least 300 ms after the fixation dot had returned to its original position.

duration and 4-Hz velocity, or 1,000-ms duration and response to the movements of the ﬁxation dot during 3-Hz velocity conditions (Table 1), as no effect of the variable ISI between the termination of the primer attention was found in these conditions (Figure 3). and onset of the test stimulus and subsequently judge whether the direction of the test stimulus was rightward or leftward. In the attentional condition (‘‘Identical’’ Procedure and ‘‘Different’’), soon after the motion direction judgment, the participants also judged whether the Each trial began with the presentation of a 1.5-s contrast of the dot that appeared after the saccades was ﬁxation point, followed by the primer (Figure 4). higher or lower than that of the original dot. Each Participants were asked to perform two saccades in session consisted of 56 trials: four trials for each of the

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Figure 5. Averaged data for each of the participant groups (the participants in Experiment 1 and the new participants) in Experiment 2. In each graph, the percentage of positive priming responses (that the test stimulus moved in the same direction as the primer) is plotted as a function of the ISI between the primer and test stimulus (in milliseconds). Each curve represents the data that were collected in the attentional conditions (‘‘Identical’’ and ‘‘Different’’ conditions) and in the condition with no attentional task (‘‘w/o task’’). Error bars represent 95% CIs. The primer durations and velocities were set to (A) 167 ms and 3 Hz and (B) 1,000 ms and 2 Hz, respectively.

seven ISIs between the priming and test stimuli (600, ‘‘Different’’), participants correctly judged whether the 800, 1,000, 1,200, 1,600, 2,000, or 3,000 ms) and for the dot contrast had decreased or increased relative to the two directions of the primer (leftward or rightward). original one (average of 95.1% correct for the The trials were presented in a random order. In each participants in Experiment 1; 94.7% correct for the new session, the durations and velocities of the primer were participants) in most of the trials. In the new fixed. The two parameter combinations (167-ms participant group, one participant correctly judged duration and 3-Hz velocity; 1,000-ms duration and 2- only 69% of the trials; therefore, his data were excluded Hz velocity) were examined. Each participant com- from the analysis. pleted four sessions for each of the two parameter Figure 5 shows the group-averaged results for each combinations, with each of the three attentional task participant group and for each condition. For both conditions in random order. Therefore, each partici- primer duration and velocity combinations, the results pant completed 32 trials per condition through 24 were similar to those obtained for the full condition in sessions in total within a month. Each session took Experiment 1, in which no saccade was required: The about 5 min to complete. Eye movements were positive priming was prominent, irrespective of whether recorded during trials. participants performed the attentional task (Figure 2). The priming effect was gradually reduced as the length of the ISIs increased. These results were robust as to Results and Discussion whether or not participants engaged in Experiment 1. For a primer duration of 167 ms and velocity of 3 Hz We verified whether the saccade was executed twice (Figure 5A), a two-way ANOVA for repeated measures synchronous to the shifts of the fixation point (the red- revealed that the main effect of the attentional task was colored dot in Figure 4). In all trials, both participant not significant, F(2, 40) ¼ 2.01, ns for the participants in groups (the participants in Experiment 1 and the new Experiment 1; F(2, 36) ¼ 0.80, ns for the new participants) made two saccades within 500 ms after the participants, whereas that of the ISI was significant, 2 offset of the primer (the duration for the two saccades F(6, 120) ¼ 72.72, p , 0.0001, g G ¼ 0.58, for the ranged from 233–489 ms for the participants in participants in Experiment 1 and F(6, 108) ¼ 39.24, p , 2 Experiment 1 and from 267–477 ms for the new 0.0001, g G ¼ 0.44 for the new participants. Further- participants). Therefore, in the ‘‘Identical’’ and ‘‘Dif- more, the interaction between the attentional task and ferent’’ attentional conditions, the dot contrast was ISI was not significant, F(12, 240) ¼ 1.00, ns for the changed after the end of the second saccade. Some participants in Experiment 1 and F(12, 216) ¼ 1.65, ns trials in which the eye position was more than 1.5% for the new participants. At a primer duration of 1,000 away from the fixation dot were excluded from the ms and velocity of 2 Hz (Figure 5B), the main effect of subsequent analysis (6.3% of trials across participants). the attentional task was not significant, F(2, 40) ¼ 0.33, In the attentional conditions (for both ‘‘Identical’’ and ns for the participants in Experiment 1 and F(2, 36) ¼

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167 ms and 3 Hz/1,000 ms and 2 Hz 167 ms and 4 Hz/1,000 ms and 3 Hz w/o task Identical Different w/o task Identical Different Experiment 1 Retinotopic No priming No priming No priming Negative Negative Negative Spatiotopic Positive only at ISI Positive No priming No priming No priming No priming of 800–1,600 ms Full Positive Positive Positive Negative Negative Negative Unmatched No priming No priming No priming No priming No priming No priming Experiment 2 Full Positive Positive Positive — — —

Table 2. The summary of the results in Experiments 1 and 2. Notes: The first row indicates the combination of the primer duration and velocity. The second row indicates three attentional conditions. The fourth, fifth, sixth, and seventh rows indicate the priming effect under the retinotopic, spatiotopic, full, and unmatched conditions in Experiment 1, respectively. The bottom row indicates the priming effect under the full condition in Experiment 2. The results affected by the attentional task are depicted in boldface font.

0.08, ns for the new participants, whereas that of the ISI Crespi et al. (2011). No effect of spatial attention was 2 was significant, F(6, 120) ¼ 113.8, p , 0.0001, g G ¼ observed on positive priming at the full condition 0.62 for the participants in Experiment 1 and F(6, 108) (Figures 2 and 5). This indicates that not the positive 2 ¼ 63.44, p , 0.0001, g G ¼ 0.52 for the new participants. priming per se but the spatiotopic motion perception is Meanwhile, the interaction between the attentional task modulated by the spatial attention. In other words, and ISI was not significant, F(12, 240) ¼ 0.12, ns for the only the stimulus configurations that contain only a participants in Experiment 1 and F(12, 216) ¼ 1.51, ns spatiotopic component combined with eye movement for the new participants. These results indicate that the but do not contain a retinotopic component were saccade per se between the priming and test stimuli affected by the attentional manipulation. cannot be the main factor for inducing the effect of As discussed in the Introduction section, whether the spatial attention observed in the spatiotopic condition blood oxygen level–dependent response of the visual in Experiment 1. cortex is tuned to spatiotopic coordinates or retinotopic coordinates is a matter of debate (Crespi et al., 2011; d’Avossa et al., 2007; Gardner et al., 2008), and it is likely that the current conflicting reports are due to the General discussion presence or absence of spatial attention to the moving stimulus or its future location (Melcher & Morrone, 2015; Zimmermann et al., 2014). Our results predict Attentional modulation of spatiotopic motion that when attention is not directed to the upcoming perception stimulus’s location, spatiotopic fMRI responses at the motion-related area may not appear; in other words, Table 2 shows the summary of the results of spatial attention is necessary to induce representation Experiments 1 and 2. We replicated the results of our for spatiotopic motion perception. previous study (Yoshimoto et al., 2014b), specifically, In the ‘‘w/o task’’ condition, in which the partici- that positive priming is dominant in the spatiotopic pants were not required to perform an attentional task, condition, whereas negative priming is prominent in the positive priming was observed for the intermediate ISIs retinotopic condition. To understand the effect of (Figure 2). The emergence of positive priming in this spatial attention on spatiotopic motion perception, we condition suggests that the participants did attend to conducted a concurrent dot contrast-change detection the location where the test stimulus would appear, even task after the saccade and found that spatial attention though they were not explicitly instructed to attend to modifies only spatiotopic motion perception. This that location. A similar argument could be applied to conclusion is supported by the findings that spatial the condition used in Crespi et al. (2011), in which the attention did not affect priming effects in the full and participants freely viewed a moving stimulus. retinotopic conditions (Figures 2, 3, and 5). When spatial attention was directed to the test When spatial attention was directed away from the stimulus position in the ‘‘Identical’’ condition of the future test stimulus location (‘‘Different’’ condition), no spatiotopic condition, the percentage of positive positive priming was observed at all in the spatiotopic priming responses increased, but only for the shorter condition. This suggests that attributing spatial atten- ISIs examined (Figure 2). In the no attentional task, tion to the future location of a test stimulus is requisite positive priming in the spatiotopic condition emerged to construct spatiotopic representation, as suggested by when the ISIs were longer than 600 ms. As described

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below, this delayed priming effect is consistent with the also that spatial attention can accelerate this process- findings that spatiotopicity develops slowly and re- ing. quires at least approximately 500 ms (e.g., Zimmer- As shown in Figure 2, the full condition was not mann et al., 2014). However, when observers were affected by the attention manipulation, even though it forced to attend to the future location of the test induced positive priming. One clear difference between stimulus, the delay observed in the ‘‘w/o task’’ the full and the spatiotopic conditions in Figure 2 is that condition almost disappeared. The results for the positive priming was clearly observed at 400 ms of ISI ‘‘Identical’’ condition indicate that the amount of delay in the full condition, whereas it was not observed in the observed in spatiotopic motion perception is not fixed spatiotopic condition in the ‘‘w/o task’’ attentional but is susceptible to the attentional condition of the condition. In the spatiotopic condition, attentional observers, as discussed below. modulation is needed to induce positive priming, as shown in the ‘‘Identical’’ condition with a short ISI of 400 or 600 ms. If the ISI-dependent positive priming Developing spatiotopic representation through effect in the spatiotopic condition indicates a slowly attention developing spatiotopic representation as previously discussed, it could be argued that spatiotopic repre- It has been argued that explicit spatiotopic representation had been already constructed in the visual sentation may not be necessary, because a mechanism pathway of participants while conducting the full that updates retinotopic information is sufficient to condition. Because participants did not have to move integrate visual information across saccades (e.g., their eye (the full condition in Experiment 1), or Cavanagh et al., 2010; Gardner et al., 2008; Merriam, because they always moved their eyes back to the Gardner, Movshon, & Heeger, 2013; Wurtz, 2008). original position (Experiment 2), spatiotopic represen- However, as described above, evidence for the existence tation did not have to be updated in those conditions, of slowly developing spatiotopic representation has which is different from the spatiotopic condition in also been amassed (Burr & Morrone, 2012; Zimmer- Experiment 1. Thus, we speculate that the needs for mann et al., 2014). For example, Zimmermann et al. temporally developing spatiotopic representation (2013) showed that a tilt aftereffect occurs in both would determine the effect of attentional modulation, retinotopic and spatiotopic conditions. They also found and the different effects of attention between the that an adaptation of tilt in the spatiotopic condition spatiotopic condition and full condition (in Experiment became effective only when the saccadic target was 1) might reflect this point. presented for 500–1,000 ms before changing gaze. Further, Golomb et al. (2011) showed that 500–600 ms is required to update spatiotopic information for each Relationship with lower- and higher-order saccade. motion mechanisms Meanwhile, Zimmerman et al. (2014) indicated that this kind of slow mechanism is relatively unrelated to The attentional effect appeared only in the spatio- the classical problem of keeping vision stable during topic condition, and no difference was observed each saccade. They suggested, rather, that the function between the ‘‘Identical’’ and ‘‘Different’’ conditions in is to store object information, including motion, in a the other reference frame conditions (Figures 2 and 3). gaze-invariant visual memory representation. Our data The reason for this absence of the attentional effect is seem to support this view, as clear positive priming, not yet clear. It can be supposed that the strength of the which is the outcome of solving the correspondence attentional modulation induced by the dot contrast- problem between the primer and test stimulus, occurs change detection task was sufficient to intervene in the after 600 ms without explicit manipulation of spatial computation of spatiotopic motion perception but was attention. Even when the attention is allocated, our not sufficient for retinotopic perception. This specula- data demonstrated a gradual increase of positive tion indicates that the processing levels for spatiotopic priming from 400 ms of ISI. This time scale seems to be and retinotopic visual motion differ, which we discuss too slow to accomplish visual stability through below. mechanisms such as efference copy or corollary Because positive and negative priming are observed discharge (e.g., Wurtz, 2008). Recently, Zimmermann, antagonistically, these two priming effects should be Weidner, Abdollahi, and Fink (2016) used a tilt induced by separate visual motion mechanisms (Kanai aftereffect and found both retinotopic and spatiotopic & Verstraten, 2005; Pantle et al., 2000). In our previous representations in visual areas such as V3, V4, and VO, experiment, negative priming became prominent in the which they examined using fMRI adaptation. Our high-velocity and low-contrast conditions, in which the study provided evidence that an attentional resource is contribution of a first-order motion system (Adelson & requisite for developing spatiotopic representation and Bergen, 1985; Lu & Sperling, 1995) increased. On the

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other hand, positive priming became dominant in the the Necker cube rivalry reflect a common mechanism low-velocity and high-contrast conditions, in which the that solves ambiguity by using the information of the high accuracy of spatial localization facilitated the priming stimulus. To understand the effects of spatial tracking of prominent visual features (Takeuchi et al., attention under different coordinates such as retino- 2011). Yoshimoto et al. (2014b) concluded that a first- topic or spatiotopic, it would be promising to clarify order system functions in retinotopic coordinates, the kind of mechanism that is functioning for these whereas a higher-order system, such as a feature- three phenomena. tracking mechanism, functions in spatiotopic coordi- Burr and Morrone (2012) discussed that spatiotopic nates. representation would be connected to action and guide This argument seems to be supported by several our physical interaction with the world. For taking existing studies that examined the relationship between appropriate actions, an internal model of the external visual motion perception and reference frames (Biber & world must be constructed and updated as we move ¨ Ilg, 2011; Boi, Ogmen, & Herzog, 2011; Cavanagh et through the world (Land, 2012). After conducting body al., 2010; Hein & Cavanagh, 2012; Knapen et al., 2009; movements, performing actions such as pointing Melcher & Morrone, 2003; Turi & Burr, 2012; precisely was possible even without visual input (Byrne, Wenderoth & Wiese, 2008). For example, Turi and Becker, & Burgess, 2007), probably by virtue of the Burr (2012) showed that lower and higher levels of spatiotopic representations of the environment con- visual information processing have different coordinate bases by using motion aftereffect and positional motion structed in our brain. In our previous study (Yoshi- aftereffect. The former, which is assumed to be moto et al., 2014a), we found that in a spatiotopic processed through a first-order system, is perceived in condition similar to the one in Figure 1, the positive retinotopic coordinates, whereas the latter, which is priming effect disappeared at dim (mesopic) light levels. assumed to require higher-order processing, is per- We speculated that these results might indicate that ceived in spatiotopic coordinates. From the results of proper spatiotopic representation was not constructed this study, it is indicated that an attentional mechanism under mesopic vision, and this kind of failure would be that modulates positive motion priming in spatiotopic related to several problems regarding the actions during coordinates functions only in the higher-order streams dusk (Yoshimoto et al., 2014a). For example, Oude- of visual motion processing. jans, Michaels, Bakker, and Davids (1999) showed that in both experimental settings and actual games, a baseball outfielder is more likely to lose sight of a flying Future studies and the relation to daily ball during dusk and commit errors. The number of environment motor vehicle accidents increases at dusk both in Japan (Yamadaya, 2010) and the United States (Owens, As described above, negative motion priming be- Wood, & Owens, 2007). comes prominent by increasing the velocity and The current study demonstrated that positive prim- presentation duration or decreasing the luminance ing at the spatiotopic condition disappeared not only contrast of the primer, whereas positive motion under mesopic conditions but also under photopic priming becomes conspicuous in the lower-velocity, conditions in which spatial attention was not directed higher-contrast, and shorter-duration priming stimulus to the stimulus. If our experimental results reflect the conditions. Other visual phenomena such as binocular function of representing object memory information in rivalry or Necker cube rivalry show similar character- a gaze-invariant manner, as suggested by Zimmermann istics to the visual motion priming (Brascamp, Knapen, et al. (2014), losing memory of objects in the Kanai, van Ee, & van den Berg, 2007; Huber & environment by the failure of constructing memory O’Reilly, 2003; Long, Toppino, & Mondin, 1992). In representation in the spatiotopic coordinates would the case of binocular rivalry, short-duration and/or induce improper actions such as making errors in low-contrast prior stimulus induces flash facilitation, catching a ball or while driving. Further studies are whereas long-duration and/or high-contrast prior needed to clarify the relationship between action, stimulus induces flash suppression (Brascamp et al., spatiotopic representations, and spatial attention. In 2007). In the Necker cube rivalry, unambiguous such studies, we would need participants to take priming cube and ambiguous Necker pattern are actions, because viewed actions such as grasping by perceived as having the same configuration when the hand are shown to be mapped retinotopically in the exposure time of the primer is short. When the visual pathway (Porat, Pertzov, & Zohary, 2011). exposure time of the primer is long, the Necker pattern is perceived to be the opposite to that of the priming Keywords: visual motion perception, reference frames, cube (Long et al., 1992). For now, we do not know spatiotopic coordinate, retinotopic coordinate, spatial whether the motion priming, the binocular rivalry, and attention, motion priming

Downloaded from jov.arvojournals.org on 05/13/2019 Journal of Vision (2019) 19(4):4, 1–19 Yoshimoto & Takeuchi 16 Acknowledgments based compression of event duration. Journal of Vision, 11(2):21, 1–9, https://doi.org/10.1167/11.2. 21. [PubMed] [Article] This work was supported by JSPS KAKENHI Grants 16K04432 and 17K13966. Burr, D. C., & Morrone, M. C. (2011). Spatiotopic coding and remapping in humans. Philosophical Commercial relationships: none. Transactions of the Royal Society of London B, 366, Corresponding authors: Sanae Yoshimoto; Tatsuto 504–515. Takeuchi. Burr, D. C., & Morrone, M. C. (2012). Constructing Email: [email protected]; [email protected]. stable spatial maps of the world. Perception, 41, ac.jp. 1355–1372. Address: Graduate School of Integrated Arts and Burr, D., Tozzi, A., & Morrone, M. C. (2007). Neural Sciences, Hiroshima University, Hiroshima, Japan; Department of Psychology, Japan Women’s mechanisms for timing visual events are spatially University, Kanagawa, Japan. selective in real-world coordinates. Nature Neuro- science, 10, 423–425. Byrne, P., Becker, S., & Burgess, N. (2007). Remem- bering the past and imagining the future: A neural References model of spatial memory and imagery. Psycholog- ical Review, 114, 340–375. Adelson, E. H., & Bergen, J. R. (1985). Spatiotemporal Campana, G., Pavan, A., & Casco, C. (2008). Priming energy models for the perception of motion. of first- and second-order motion: Mechanisms and Journal of the Optical Society of America A, 2, 284– neural substrates. Neuropsychologia, 46, 393–398. 299. Cavanagh, P., Hunt, A. R., Afraz, A., & Rolfs, M. Anstis, S. M. (1980). The perception of apparent (2010). Visual stability based on remapping of movement. Philosophical Transactions of the Royal attention pointers. Trends in Cognitive Sciences, 14, Society of London B, 290, 153–168. 147–153. Anstis, S., & Ramachandran, V. S. (1987). Visual inertia in apparent motion. Vision Research, 27, Cohen, J. (1988). Statistical power analysis for the 755–764. behavioral sciences (2nd ed.). New York: Academic Press. Bakeman, R. (2005). Recommended effect size statistics for repeated measures designs. Behaviour Research Crespi, S., Biagi, L., d’Avossa, G., Burr, D. C., Tosetti, Methods, 37, 379–384. M., & Morrone, M. C. (2011). Spatiotopic coding of BOLD signal in human visual cortex depends on Biber, U., & Ilg, U. J. (2011). Visual stability and the spatial attention. PLoS One, 6, e21661. motion aftereffect: A psychophysical study reveal- ing spatial updating PLoS One, 6, e16265. d’Avossa, G., Tosetti, M., Crespi, S., Biagi, L., Burr, D. C., & Morrone, M. C. (2007). Spatiotopic Boi, M., O¨ gmen, H., & Herzog, M. H. (2011). Motion selectivity of BOLD responses to visual motion in and tilt aftereffects occur largely in retinal, not in object, coordinates in the Ternus-Pikler display. human area MT. Nature Neuroscience, 10, 249–255. Journal of Vision, 11(3):7, 1–11, https://doi.org/10. Duhamel, J. R., Colby, C. L., & Goldberg, M. E. (1992, 1167/11.3.7. [PubMed] [Article] January 3). The updating of the representation of Braddick, O. J. (1980). Low-level and high-level visual space in parietal cortex by intended eye processes in apparent motion. Philosophical Trans- movements. Science, 255, 90–92. actions of the Royal Society of London B, 290, 137– Ezzati, A., Golzar, A., & Afraz, A. S. R. (2008). 151. Topography of the motion aftereffect with and Brainard, D. H. (1997). The Psychophysics Toolbox. without eye movements. Journal of Vision, 8(14):23, Spatial Vision, 10, 433–436. 1–16, https://doi.org/10.1167/8.14.23. [PubMed] [Article] Brascamp, J. W., Knapen, T. H., Kanai, R., van Ee, R., & van den Berg, A. V. (2007). Flash suppression Fernandez, G. C. J. (1992). Residual analysis and data and flash facilitation in binocular rivalry. Journal of transformations: Important tools in statistical Vision, 7(12):12, 1–12, https://doi.org/10.1167/7.12. analysis. HortScience, 27, 297–300. 12. [PubMed] [Article] Fracasso, A., Caramazza, A., & Melcher, D. (2010). Burr, D. C., Cicchini, G. M., Arrighi, R., & Morrone, Continuous perception of motion and shape across M. C. (2011). Spatiotopic selectivity of adaptation- saccadic eye movements. Journal of Vision, 10(13):

Downloaded from jov.arvojournals.org on 05/13/2019 Journal of Vision (2019) 19(4):4, 1–19 Yoshimoto & Takeuchi 17

14, 1–17, https://doi.org/10.1167/10.13.14. reference frame of the motion aftereffect is reti- [PubMed] [Article] notopic. Journal of Vision, 9(5):16, 1–6, https://doi. Gardner, J. L., Merriam, E. P., Movshon, J. A., & org/10.1167/9.5.16. [PubMed] [Article] Heeger, D. J. (2008). Maps of visual space in Knapen, T., Rolfs, M., Wexler, M., & Cavanagh, P. human occipital cortex are retinotopic, not spatio- (2010). The reference frame of the tilt aftereffect. topic. Journal of Neuroscience, 28, 3988–3999. Journal of Vision, 10(1):8, 1–13, https://doi.org/10. Ghodrati, M., Morris, A. P., Price, N. S. (2015). The 1167/10.1.8. [PubMed] [Article] (un)suitability of modern liquid crystal displays Krauzlis, R. J., & Miles, F. A. (1996). Release of (LCDs) for vision research. Frontiers in Psychology, fixation for pursuit and saccades in humans: 6, 303. Evidence for shared inputs acting on different Golomb, J. D., Marino, A. C., Chun, M. M., & Mazer, neural substrates. Journal of Neurophysiology, 76, J. A. (2011). Attention doesn’t slide: Spatiotopic 2822–2833. updating after eye movements instantiates a new, Land, M. F. (2012). The operation of the visual system discrete attentional locus. Attention, Perception & in relation to action. Current Biology, 22, R811– Psychophysics, 73, 7–14. R817. Golomb, J. D., Nguyen-Phuc, A. Y., Mazer, J. A., Long, G. M., Toppino, T. C., & Mondin, G. W. (1992). McCarthy, G., & Chun, M. M. (2010). Attentional Prime time: Fatigue and set effects in the perception facilitation throughout human visual cortex lingers of reversible figures. Perception & Psychophysics, in retinotopic coordinates after eye movements. 52, 609–616. Journal of Neuroscience, 30, 10493–10506. Lu, Z. L., & Sperling, G. (1995). The functional Golomb, J. D., Pulido, V. Z., Albrecht, A. R., Chun, architecture of human visual motion perception. M. M., & Mazer, J. A. (2010). Robustness of the Vision Research, 35, 2697–2722. retinotopic attentional trace after eye movements. Marino, A. C., & Mazer, J. A. (2016). Perisaccadic Journal of Vision, 10(3):19, 1–12, https://doi.org/10. updating of visual representations and attentional 1167/10.3.19. [PubMed] [Article] states: Linking behavior and neurophysiology. Hein, E., & Cavanagh, P. (2012). Motion correspon- Frontiers in Systems Neuroscience, 10,3. dence in the Ternus display shows feature bias in Mathoˆt, S., & Theeuwes, J. (2010). Gradual remapping spatiotopic coordinates. Journal of Vision, 12(7):16, results in early retinotopic and late spatiotopic 1–14, https://doi.org/10.1167/12.7.16. [PubMed] inhibition of return. Psychological Science, 21, [Article] 1793–1798. Heller, N. H., & Davidenko, N. (2018). Dissociating Melcher, D. (2005). Spatiotopic transfer of visual-form higher and lower order visual motion systems by adaptation across saccadic eye movements. Current priming illusory apparent motion. Perception, 47, Biology, 15, 1745–1748. 30–43. Melcher, D., & Colby, C. L. (2008). Trans-saccadic Helmholtz, H. (1867). Handbuch der physiologischen perception. Trends in Cognitive Sciences, 12, 466– optik (Vol. 9). Leipzig, Germany: Voss. 473. Huber, D. E., & O’Reilly, R. C. (2003). Persistence and Melcher, D., & Fracasso, A. (2012). Remapping of the accommodation in short-term priming and other line motion illusion across eye movements. Exper- perceptual paradigms: Temporal segregation imental Brain Research, 218, 503–514. through synaptic depression. Cognitive Science, 27, Melcher, D., & Morrone, M. C. (2003). Spatiotopic 403–430. temporal integration of visual motion across Jiang, Y., Luo, Y. J., & Parasuraman, R. (2002). saccadic eye movements. Nature Neuroscience, 6, Neural correlates of perceptual priming of visual 877–881. motion. Brain Research Bulletin, 57, 211–219. Melcher, D., & Morrone, M. C. (2015). Nonretinotopic Jiang, Y., Pantle, A. J., & Mark, L. S. (1998). Visual visual processing in the brain. Visual Neuroscience, inertia of rotating 3-D objects. Perception & 32, e017. Psychophysics, 60, 275–286. Merriam, E. P., Gardner, J. L., Movshon, J. A., & Kanai, R., & Verstraten, F. A. (2005). Perceptual Heeger, D. J. (2013). Modulation of visual manifestations of fast neural plasticity: Motion responses by gaze direction in human visual cortex. priming, rapid motion aftereffect and perceptual Journal of Neuroscience, 33, 9879–9889. sensitization. Vision Research, 45, 3109–3116. Morrone, M. C., Cicchini, M., & Burr, D. C. (2010). Knapen, T., Rolfs, M., & Cavanagh, P. (2009). The Spatial maps for time and motion. Experimental

Downloaded from jov.arvojournals.org on 05/13/2019 Journal of Vision (2019) 19(4):4, 1–19 Yoshimoto & Takeuchi 18

Brain Research, 206, 121–128, https://doi.org/10. 11(12):17, 1–22, https://doi.org/10.1167/11.12.17. 1007/s00221-010-2334-z. [PubMed] [Article] Nieman, D. R., Hayashi, R., Andersen, R. A., & Ramachandran, V. S., & Anstis, S. M. (1983). Shimojo, S. (2005). Gaze direction modulates visual Extrapolation of motion path in human visual aftereffects in depth and color. Vision Research, 45, perception. Vision Research, 23, 83–85. 2885–2894, https://doi.org/10.1016/j.visres.2005.06. Raymond, J. E., O’Donnell, H. L., & Tipper, S. P. 029. (1998). Priming reveals attentional modulation of Olejnik, S., & Algina, J. (2003). Generalized eta and human motion sensitivity. Vision Research, 38, omega squared statistics: Measures of effect size for 2863–2867. some common research designs. Psychological Seidel Malkinson, T., McKyton, A., & Zohary, E. Methods, 8, 434–447. (2012). Motion adaptation reveals that the motion Ong, W. S., Hooshvar, N., Zhang, M., & Bisley, J. W. vector is represented in multiple coordinate frames. (2009). Psychophysical evidence for spatiotopic Journal of Vision, 12(6):30, 1–11, https://doi.org/10. processing in area MT in a short-term memory for 1167/12.6.30. [PubMed] [Article] motion task. Journal of Neurophysiology, 102, Sommer, M. A., & Wurtz, R. H. (2002, May 24). A 2435–2440. pathway in primate brain for internal monitoring of movements. Science, 296, 1480–1482. Oudejans, R. R., Michaels, C. F., Bakker, F. C., & Davids, K. (1999). Shedding some light on catching Takeuchi, T., Tuladhar, A., & Yoshimoto, S. (2011). in the dark: Perceptual mechanisms for catching fly The effect of retinal illuminance on visual motion balls. Journal of Experimental Psychology: Human priming. Vision Research, 51, 1137–1145. Perception and Performance, 25, 531–542. Turi, M., & Burr, D. (2012). Spatiotopic perceptual Owens, D. A., Wood, J. M., & Owens, J. M. (2007). maps in humans: Evidence from motion adapta- Effects of age and illumination on night driving: A tion. Proceedings of the Royal Society B, 279, 3091– road test. Human Factors, 49, 1115–1131. 3097. van Santen, J. P., & Sperling, G. (1984). Temporal Pantle, A. J., Gallogly, D. P., & Piehler, O. C. (2000). covariance model of human motion perception. Direction biasing by brief apparent motion stimuli. Journal of the Optical Society of America A, 1, 451– Vision Research, 40, 1979–1991. 473. Pavan, A., Campana, G., Guerreschi, M., Manassi, M., Wandell, B. A., Brewer, A. A., & Dougherty, R. F. & Casco, C. (2009). Separate motion-detecting (2005). Visual field map clusters in human cortex. mechanisms for first- and second-order patterns Philosophical Transactions of the Royal Society of revealed by rapid forms of visual motion priming London B, 360, 693–707. and motion aftereffect. Journal of Vision, 9(11):27, 1–16, https://doi.org/10.1167/9.11.27. [PubMed] Watson, A. B., & Ahumada, A. J., Jr. (1985). Model of Journal of the [Article] human visual-motion sensing. Optical Society of America A, 2, 322–341. Pavan, A., & Skujevskis, M. (2013). The role of Wenderoth, P., & Wiese, M. (2008). Retinotopic stationary and dynamic test patterns in rapid forms encoding of the direction aftereffect. Vision Re- Journal of Vision 13 of motion after-effect. , (1):10, search, 48, 1949–1954. 1–17, https://doi.org/10.1167/13.1.10. [PubMed] [Article] Wurtz, R. H. (2008). Neuronal mechanisms of visual stability. Vision Research, 48, 2070–2089. Pelli, D. G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into Yamadaya, K. (2010, September). Road traffic acci- movies. Spatial Vision, 10, 437–442. dents in 2010. In T. Fujikawa (Chair), The 2nd committee meeting on Department of Traffic Acci- Piehler, O. C., & Pantle, A. J. (2001). Direction-specific dent. Symposium conducted at the Institution of changes of sensitivity after brief apparent motion Automobile Technology, Tokyo, Japan. stimuli. Vision Research, 41, 2195–2205. Yoshimoto, S., & Takeuchi, T. (2013). Visual motion Pinkus, A., & Pantle, A. (1997). Probing visual motion priming reveals why motion perception deteriorates signals with a priming paradigm. Vision Research, during mesopic vision. Journal of Vision, 13(8):8, 1– 37, 541–552. 21, https://doi.org/10.1167/13.8.8. [PubMed] Porat, Y., Pertzov, Y., & Zohary, E. (2011). Viewed [Article] actions are mapped in retinotopic coordinates in Yoshimoto, S., Uchida-Ota, M., & Takeuchi, T. the human visual pathways. Journal of Vision, (2014a). Effect of light level on the reference frames

Downloaded from jov.arvojournals.org on 05/13/2019 Journal of Vision (2019) 19(4):4, 1–19 Yoshimoto & Takeuchi 19

of visual motion processing. Journal of Vision, and across eye-movements. Behavioral Brain Re- 14(13):6, 1–28, https://doi.org/10.1167/14.13.6. search, 275, 281–287. [PubMed] [Article] Zimmermann, E., Morrone, M. C., Fink, G. R., & Yoshimoto, S., Uchida-Ota, M., & Takeuchi, T. Burr, D. (2013). Spatiotopic neural representations (2014b). The reference frame of visual motion develop slowly across saccades. Current Biology, priming depends on underlying motion mechanisms. Journal of Vision, 14(1):10, 1–19, https://doi. 23, R193–R194. org/10.1167/14.1.10. [PubMed] [Article] Zimmermann, E., Weidner, R., Abdollahi, R. O., & Zimmermann, E., Morrone, M. C., & Burr, D. C. Fink, G. R. (2016). Spatiotopic adaptation in visual (2014). Buildup of spatial information over time areas. Journal of Neuroscience, 36, 9526–9534.

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