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Smooth Anticipatory Eye Movements Alter the Memorized Position of Flashed Targets

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Smooth Anticipatory Eye Movements Alter the Memorized Position of Flashed Targets Journal of Vision (2003) 3, 761-770 http://journalofvision.org/3/11/10/ 761 Smooth anticipatory eye movements alter the memorized position of flashed targets Center for Systems Engineering and Applied Mechanics and Laboratory of Neurophysiology, Université catholique Gunnar Blohm de Louvain, Louvain-la-Neuve, Belgium Laboratory of Neurophysiology, Université catholique de Marcus Missal Louvain, Brussels, Belgium Center for Systems Engineering and Applied Mechanics and Laboratory of Neurophysiology, Université catholique Philippe Lefèvre de Louvain, Louvain-la-Neuve, Belgium Briefly flashed visual stimuli presented during smooth object- or self-motion are systematically mislocalized. This phenomenon is called the “flash-lag effect” (Nijhawan, 1994). All previous studies had one common characteristic, the subject’s sense of motion. Here we asked whether motion perception is a necessary condition for the flash-lag effect to occur. In our first experiment, we briefly flashed a target during smooth anticipatory eye movements in darkness and subjects had to orient their gaze toward the perceived flash position. Subjects reported to have no sense of eye motion during anticipatory movements. In our second experiment, subjects had to adjust a cursor on the perceived position of the flash. As a result, we show that gaze orientation reflects the actual perceived flash position. Furthermore, a flash-lag effect is present despite the absence of motion perception. Moreover, the time course of gaze orientation shows that the flash- lag effect appeared immediately after the egocentric to allocentric reference frame transformation. Keywords: anticipation, smooth pursuit, saccades, localization, flash perception, flash-lag effect One condition in which localization errors happen is Introduction during smooth object- or self-motion. An impressive It seems natural that in our everyday life, we demonstration of such a perceptual mislocalization has experience the visual environment to be spatially stable. first been conducted by MacKay (1958) and has later been However, when we orient gaze or move through the visual rediscovered by Nijhawan (1994). In their experiment, scene, self-motion induces an optic flow. Thus, for a two strobed segments that were flashed in alignment with stable space perception during self-motion, the central a continuously lit rotating line lagged the moving object, nervous system (CNS) has to use extraretinal signals to and the size of the lag increased with angular velocity. compensate for retinal motion. In this condition, the This phenomenon is called the “flash-lag effect” and has question arises, “How does the brain combine visual been extensively studied using the original, rotational signals from the environment with internal signals related configuration (Brenner & Smeets, 2000; Eagleman & to self-motion?” Sejnowski, 2000; Krekelberg & Lappe, 1999; Lappe & An interesting way to address the issue of a stable Krekelberg, 1998; Purushothaman, Patel, Bedell, & percept of the environment is to perform a localization Ogmen, 1998), as well as using constant linear motion task. To localize a flashed object, the brain has to (Brenner, Smeets, & van den Berg, 2001; Whitney, integrate the object’s retinal location with an extra-retinal Cavanagh, & Murakami, 2000; Whitney & Murakami, signal about the direction of gaze (Bridgeman, 1995; 1998). However, the flash-lag effect is not restricted to Festinger & Canon, 1965; Mergner, Nasios, Maurer, & moving objects but also appears during smooth pursuit Becker, 2001; Mon-Williams & Tresilian, 1998; van eye movements (Kerzel, 2000; Nijhawan, 2001; van Beers Beers, Wolpert, & Haggard, 2001). It is particularly et al., 2001). This is also the case for head or whole body difficult for the CNS to match moving and flashed movements (Schlag, Cai, Dorfman, Mohempour, & stimuli because continuously changing variables (i.e., Schlag-Rey, 2000). In both conditions, retinal signals position and velocity signals) have to be matched at key about motion are absent. Even more spectacular is the events, although they are processed with different delays. finding that in certain conditions a flash-lag appears A systematic bias of the perceived position shows the without any motion at all. Illusory motion perception can limits of this process (for a review, see Schlag & Schlag- induce a perceptual bias of a flashed target (Cai, Rey, 2002). doi:10.1167/3.11.10 Received March 21, 2003; published December 4, 2003 ISSN 1534-7362 © 2003 ARVO Blohm, Missal, & Lefèvre 762 Jacobson, Baloh, Schlag-Rey, & Schlag, 2000; Nishida & moving 0.2° red laser target was back-projected onto the Johnston, 1999; Watanabe, Nijhawan, & Shimojo, 2002). screen. The target was controlled via an M3-Series mirror The flash-lag effect shows two characteristic features. galvanometer (GSI Lumonics) and by using a dedicated First, there is a difference in flash localization error computer running LabViewRT (National Instruments, depending on the retinal location of the flash with respect Austin, TX, USA) software. Movements of one eye were to the motion direction (i.e., a flash presented ahead or recorded with the scleral coil technique, Skalar Medical behind the gaze direction is mislocalized differently) BV (Collewijn, van der Mark, & Jansen, 1975; Robinson, (Kerzel, 2000; Nijhawan, 2001; van Beers et al., 2001; 1963). Whitney et al., 2000; Whitney & Murakami, 1998). Paradigm Second, the final gaze orientation error depends linearly on the eye and/or target velocity at the moment of the Recording sessions were composed of a series of flash (Brenner et al., 2001; Nijhawan, 2001; van Beers et blocks, each containing 40 trials. During the first block of al., 2001). trials, the moving target was always present. These trials In all previous studies of the flash-lag effect, it could were used to build up an anticipatory response and will be hypothesized that it was exclusively due to the be referred to as build-up trials. After one block of build- perception of motion. In these experiments, a perception up trials, several blocks of test trials randomly mixed with of motion was induced either by target motion, self- build-up trials were presented. motion, or illusory motion. Is motion perception Build-up trials (Figure 1A) started with an 800-ms necessary to evoke a flash-lag? Here we tested whether a fixation period at the center of the screen. After a 300-ms flash-lag could be induced by self-motion but in the target extinction period (gap), the target moved from the absence of motion perception. This was done by testing center of the screen for 800-ms at 40°/s, always in the subjects in a situation where there is no perception of same direction. The trial ended with another 500-ms motion despite smooth anticipatory eye movements. In fixation period. The gap duration was chosen to provide our first experiment, we designed a paradigm inducing an optimal smooth anticipatory eye movement (Morrow smooth anticipatory eye movements that were not & Lamb, 1996). perceived by subjects (Kowler & Steinman, 1979). During these smooth eye movements, we presented briefly a flashed target and asked subjects to orient gaze toward the A remembered target position. In our second experiment, 800ms, 0º we validated our gaze orientation approach by a perceptual localization task. As a result, we rule out the hypothesis that the bias in spatial perception is due to 300ms, gap motion perception. Indeed, we show that spatial perception of human subjects can be altered by self- 800ms, 40º/s motion in the absence of the sense of motion. 500ms, 32º Methods B Experiment 1 800ms, 0º 100-500ms, gap Experimental set-up Healthy human subjects without any known oculomotor abnormalities participated in the experiment 10ms, [-15º..15º] after informed consent. Among the seven subjects, three were completely naïve of oculomotor experiments. Mean 1.100-1.500ms age was 29 years, ranging from 22 to 36 years. All procedures were conducted with approval of the Université catholique de Louvain Ethics Committee, in compliance with the Helsinki declaration (1996). Experiments were conducted in a completely dark Figure 1. Experimental paradigm. A. Build-up trials. After an room. Subjects sat in front of a 1-m distant tangent 800-ms fixation and a 300 ms gap period, the target moved screen, which spanned about ±45° of their visual field. for 800 ms at 40°/s, always in the same direction. B. Test Their heads were restrained by a chin-rest. A horizontally trials. Test trials started like build-up trials with an 800-ms fixation. After a variable gap of 100-500 ms, a 10-ms flash appeared at a random position between -15° and 15°. Blohm, Missal, & Lefèvre 763 In the second part of the recording session, build-up trials were randomly interleaved with 30% of test trials 20 flash Eye (Figure 1B). Test trials started in the same way as build-up 15 trials with an 800-ms fixation period in the center of the 10 PE(t) screen. Afterwards, instead of the fixed gap followed by a flash 5 ramp target motion, the target disappeared for a random PE EV duration lasting between 100 and 500-ms. This variable Position (deg) flash 0 gap was followed by a 10-ms flash presented at a random position ±15° around the expected eye position (= target 0 500 500 position of build-up trials). All trials lasted for 2400-ms. Subjects were instructed to follow the target as accurately Time (ms) as possible during build-up trials, and to orient gaze to the Figure 2. Data analysis. After the occurrence of the first memorized target (flash) position during test trials. orientation saccade, eye position error (PE) was sampled Data acquisition and analysis every 50 ms. Dotted black lines represent the initial fixation point and the flash position. The star stands for the flash. The Eye and target position were sampled at 500-Hz and red line represents eye position (saccades in bold). At the stored on the hard disk of a PC for offline analysis with moment of the flash, position error (PEflash) and eye velocity Matlab (Mathworks) scripts.
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