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Looking Ahead: the Perceived Direction of Gaze Shifts Before the Eyes Move

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Looking Ahead: the Perceived Direction of Gaze Shifts Before the Eyes Move Journal of Vision (2009) 9(9):1, 1–7 http://journalofvision.org/9/9/1/ 1 Looking ahead: The perceived direction of gaze shifts before the eyes move School of Psychology, University of Aberdeen, Aberdeen, UK,& Vision Sciences Lab, Department of Psychology, Amelia R. Hunt Harvard University, Cambridge, MA, USA Laboratoire Psychologie de la Perception, Université Paris Descartes, Paris, France,& Vision Sciences Lab, Department of Psychology, Patrick Cavanagh Harvard University, Cambridge, MA, USA How do we know where we are looking? Our direction of gaze is commonly thought to be assigned to the location in the world that falls on our fovea, but this may not always hold, especially, as we report here, just before an eye movement. Observers shifted their gaze to a clock with a fast-moving hand and reported the time perceived to be on the clock when their eyes first landed. The reported time was 39 ms earlier than the actual time the eyes arrived. In a control condition, the clock moved to the eyes, mimicking the retinal motion but without the eye movement. Here the reported time lagged 27 ms behind the actual time on the clock when it arrived. The timing of perceived fixation in our experiment is similar to that for the predictive activation observed in visual cortex neurons at the time of eye movements. Keywords: eye movements, stable perception, consciousness Citation: Hunt, A. R., & Cavanagh, P. (2009). Looking ahead: The perceived direction of gaze shifts before the eyes move. Journal of Vision, 9(9):1, 1–7, http://journalofvision.org/9/9/1/, doi:10.1167/9.9.1. associated with eye movement control (Sommer & Wurtz, Introduction 2002, 2006) Together these findings have supported the idea that a pre-saccadic signal from the oculomotor As the eyes move around, the point in the visual world system allows the visual system to predict and discount that lands on our fovea shifts. It is commonly assumed spatial changes produced by an eye movement (see that our perceived direction of gaze moves to that new Helmholtz, 1890; Sperry, 1950; von Holst & Mittelstaedt, point. This sense that it is our direction of gaze that shifted 1950). and not the world is an important component in seeing If the predictive activation of receptive fields is part of the world as stable despite displacement of the retinal the processes that stabilize the visual world, we may also image caused by eye movements. see a shift in the perceived direction of gaze just before an Cell recordings at the time of eye movements in a wide eye movement. This would suggest that the sensed range of visual areas, including striate and extrastriate direction of gaze is attributed to the predicted location of cortex (Nakamura & Colby, 2002; see also Merriam, the fovea. Previous work is suggestive; Deubel, Irwin, and Genovese, & Colby, 2007), Lateral Interparietal cortex Schneider (1999) found that a probe flash had to precede a (LIP, Duhamel, Colby, & Goldberg, 1992), and the saccade by as much as 250 msec to be judged as Frontal Eye Fields (FEF, Sommer & Wurtz, 2002, simultaneous with the arrival at the saccade target. This 2006), have demonstrated that a proportion of visual cells large delay is far outside the range of predictive remap- in these regions respond to stimuli that will fall in their ping, but the experiment required subjects to judge the receptive fields before the eyes move to bring them there. relative timing of a flashed probe and an eye movement, The majority of these cells begin responding at the time of and the difficulty of shifting attention between the probe the saccade, or just following it, showing responses that and the saccade events may have contributed to the size of are too early to be driven by the actual arrival of the the effect. We used a more direct measure of the perceived stimulus in their receptive field (Kusunoki & Goldberg, time of arrival at a saccade target and we find a delay 2002). In other words, the consequence of each eye more consistent with the range found for remapping. We movement is simulated in many visual areas ahead of the presented a large clock with single hand rotating at 1 rps actual movement. The signal to remap receptive fields (see Carlson, Hogendoorn, & Verstraten, 2006)asa arises, at least in part, from a pathway to FEF that saccade target. Observers made an 8- saccade to the originates in the Superior Colliculus, which is closely clock, noted the time they arrived, and then adjusted a doi: 10.1167/9.9.1 Received April 23, 2009; published August 10, 2009 ISSN 1534-7362 * ARVO Journal of Vision (2009) 9(9):1, 1–7 Hunt & Cavanagh 2 second clock to match this perceived arrival time (see 4- to the left of the center of the screen, and a clock face with Figure 1). Observers reported that it was easy to tell when a4.4- diameter, with its center positioned 4- to the right of they began looking at the clock as opposed to still viewing the center of the screen. The clock had a single clock hand it at 8- in the periphery. The physical arrival time was pointed in a randomly selected direction. After the observer taken as the position of the clock hand at the moment the pressed the space bar and a stable fixation was detected, the eye monitor showed the eyes had landed on the clock. hand began spinning in a clockwise direction at a rate of Thus we can observe the time that observers judged they 1 rps. After 330 ms, a beep signaled the observer to make an were looking at the clock relative to when they actually eye movement to the clock face. The clock continued to spin did arrive. To control for various sources of lead or lag in for 670 ms, and then the screen cleared and a new clock was reported arrival time, in a second condition the task and presented at the center of the screen with the hand pointed in stimuli were the same, but the eyes remained steady and a randomly selected direction, and the words “use l/r arrows the clock moved to fixation, mimicking the retinal motion to adjust and press space” printed above, instructing the of the clock without an eye movement. observer to use the left and right arrow keys to move the clock hand to the time they remembered to be on the clock when the eyes arrived on its face (see Figure 1). Trials were rejected if the first eye movement was not executed in the Main clock experiment interval between the saccade signal and the termination of the clock (10.8% of trials), or if the first eye movement did Methods not land on the face of the clock (11.2% of remaining trials). The remaining saccades had a mean landing position Each of the 8 observers (one was the first author, the others 2 mm to the right and 4 mm below the actual center of the were recruited from the Harvard Vision Lab) was seated in a clock, with a standard error of less than 1 mm. The actual dimly lit room, viewing a 20-inch, 85 Hz monitor from a arrival time of the eyes was defined as the time on the clock chin rest positioned 37 cm away. Movements of the right eye when the eye movement velocity dropped below the - only were monitored using a 120 Hz Eyelink I monitor (SR saccade detection threshold of 30 per second (and the trial Research, Canada). Experimental sessions consisted of a was only included in the analysis if the eyes were on the block of 80 experimental and block of 80 control trials, with clock when this threshold was crossed). order counterbalanced across observers. Each block began The control condition was the same, except that the with a 9-point calibration sequence. The initial display was a observer remained fixated and the clock face moved to fixation circle (a black annulus) on a 50% gray background, fixation. In a pilot version of the main experiment, saccade latencies to execute an eye movement to the clock had a mean of 235 ms, a standard deviation of 114 ms, and a duration of 42 ms. Therefore, the latency from the onset of the beep to the onset of the clock’s movement to fixation was selected on each trial from a distribution with this mean and standard deviation to approximate the same timing parameters as the saccade condition. The duration of the motion was 47 ms (i.e., 6 frames). The observer was instructed to remain fixated throughout each trial, and to judge the time that was on the clock when it arrived at fixation. Trials were rejected if a saccade was detected before the clock arrived at fixation. These accounted for 5% of trials. Results Results are shown in Figure 2. Average perceived arrival time in the saccade condition was 39 ms earlier than the actual time on the clock when the eyes arrived, and reported arrival times that were earlier than the actual arrival time comprised 67% of reports (20% of reports were times that occurred when the eyes were actually in motion). In the control condition, perceived arrival lagged Figure 1. A. Observer saccades to a clock with a spinning hand. behind the actual arrival by 27 ms, a delay likely related B. Observer moves the hand to the position it was in when the to the flash-lag effect (that is, the perceived position of a eyes landed on the clock face.
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