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Neuronal Latencies and the Position of Moving Objects Review TRENDS in Neurosciences Vol.24 No.6 June 2001 335 Neuronal latencies and the position of moving objects Bart Krekelberg and Markus Lappe Neuronal latencies delay the registration of the visual signal from a moving flashed object, either because it does not move, or object. By the time the visual input reaches brain structures that encode its because its duration is too short to initiate position, the object has already moved on. Do we perceive the position of a extrapolation mechanisms. Hence, the flash is seen at moving object with a delay because of neuronal latencies? Or is there a brain its true position, but the moving object is seen at an mechanism that compensates for latencies such that we perceive the true extrapolated position (Fig. 2b). This extrapolated position of a moving object in real time? This question has been intensely position is the position the moving object occupies debated in the context of the flash-lag illusion: a moving object and an object ‘now’, not the position it occupied when the flash hit flashed in alignment with it appear to occupy different positions. The moving the retina: hence, the flash will appear to lag behind. object is seen ahead of the flash. Does this show that the visual system If motion extrapolation compensates for neuronal extrapolates the position of moving objects into the future to compensate for latencies, the magnitude of the lag-effect should neuronal latencies? Alternative accounts propose that it simply shows that depend on the actual latency of the moving object. moving and flashed objects are processed with different delays, or that it Hence, a crucial test manipulates the latency of the reflects temporal integration in brain areas that encode position and motion. moving object and determines whether the lag co- The flash-lag illusion and the hypotheses put forward to explain it lead to varies. Neuronal latency increases when stimulus interesting questions about the encoding of position in the brain. Where is the luminance decreases8,9. Therefore, when the ‘where’ pathway and how does it work? luminance of the moving object in the flash-lag illusion is decreased, the lag should increase to In the flash-lag illusion, observers compare the compensate for the increased latency. Contrary to this position of a continuously moving stimulus to the prediction, however, the lag decreases with a decrease position of a brief flash of light. When the moving in luminance3 and can even turn into a flash-lead10. stimulus and the flashed stimulus are physically Moreover, motion extrapolation should become aligned in space and time, observers nonetheless incorrect when a moving object abruptly reverses perceive a spatial offset: the moving stimulus appears direction; it should yield apparent positions beyond advanced relative to the position of the flashed the reversal point. This, however, is not observed stimulus (Fig. 1). experimentally2,11,12. The failure to compensate for Earlier reports of similar phenomena can be found latency variations correctly and the lack of a as far back as the 1920s (Refs 5–7). But Nijhawan’s predicted overshoot has prompted several rediscovery and new interpretation in 1994 created a researchers to look for alternative explanations of the surge of interest, certainly because we now know flash-lag effect. much more about the neural processes underlying perception, appreciate the problem of neural latencies Differential latencies and have psychophysical as well as The differential latencies hypothesis proposes that neurophysiological tools to unravel the mechanisms the flash-lag effect occurs simply because the visual that underlie these phenomena. This article discusses system responds with a shorter latency to moving the properties of the flash-lag effect known from a stimuli than to flashed stimuli2,10,11. Thus, temporal host of studies carried out since Nijhawan’s report. coincidence of the neural representation of the two The hypotheses on the origin of the flash-lag effect stimuli occurs when the moving stimulus is farther will be discussed mainly in the light of these along its path rather than when both stimuli coincide psychophysical findings. It is important, however, to physically (Fig. 2c). put the psychophysical hypotheses on a The differential latencies hypothesis provides a neurophysiological basis, and review some of the natural explanation for the linear speed dependence pertinent data. of the flash-lag effect (Fig. 1c). The linearity simply reflects that the difference in latency is independent Bart Krekelberg* Motion extrapolation of speed. In addition, because a reduction in Markus Lappe Nijhawan has proposed that the visual system uses luminance of the moving object reduces the difference Dept of Zoology and Neurobiology, Ruhr- the motion signals to extrapolate the position of a in latencies, this hypothesis easily incorporates the University Bochum, moving object1. Accordingly, the representation findings discussed above. 44780 Bochum, Germany. faithfully reflects the position of the object at the time If a flashed object indeed has a longer latency than *e-mail: bart@ neurobiologie.ruhr-uni- it is perceived and, as such, compensates for neuronal a moving object, one would expect this to be reflected bochum.de delays. Extrapolation cannot occur for a briefly in temporal order judgements. Eagleman and http://tins.trends.com 0166-2236/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0166-2236(00)01795-1 336 Review TRENDS in Neurosciences Vol.24 No.6 June 2001 (a) (b) (c) 25 20 ) ° 15 10 Lag ( Delay = 70 ms 5 Real Perceived 0 0 50 100 150 200 250 Speed (°/s) TRENDS in Neurosciences Fig. 1. The flash-lag illusion1. (a) The stimulus. A bar (shown in red) Attentional delays moves. A second bar (shown in blue) is flashed in perfect alignment. Differences in latencies could arise not only from the (b) The percept: the moving bar (red) appears to be ahead of the flashed properties of single neurones, but also from higher bar (blue). Note that the illusion is not because observers fail to stick to the instructions and report the alignment of flash-offset (which could level processing. For example, the flash could trigger possibly be delayed as a result of persistence of the flash) with the an attentional process to estimate the position of the moving stimulus. Whitney et al. convincingly demonstrated this by flash. This process takes time and by the time the extending the flash-duration as well as by backward masking2. For technical reasons most studies have used rotating line segments rather system gets round to judging the position of the than the linear motion shown here. The illusion is strong in both cases. moving object, the latter will have moved on and a Moreover, the flashed object does not have to be stationary. A flash-lag spatial offset will be perceived14–16. also occurs between a continuously lit moving object and another To test whether attention plays a role in the flash- moving object that is visible only briefly3 or intermittently4. (c) The magnitude of the offset depends linearly on the speed of the moving lag effect, several authors have used paradigms that object. The slope of the speed dependence can be used to express compare the lag in situations where the occurrence of spatial offsets as equivalent temporal delays. In Nijhawan’s the flash is predictable or unpredictable. experiments1, the perceived spatial offset corresponded to a time difference of about 80 ms, roughly the typical latency of early visual Unfortunately, the results are mixed: although some 15 23 cortical neurones. In this figure, the equivalent delay is 70 ms authors report that cueing or predictability of the (Fig. based on data published in Ref. 3). flash reduces the lag, others claim that there is no attentional effect17. Sejnowski have tested this by flashing a bar at the time a moving bar came to a halt. Subjects perceived Temporal integration the temporal order of these events correctly. But, as The temporal averaging model proposes that the earlier experiments have shown that there is no flash- visual system collects position signals over time and lag effect at motion offset12, this experiment does not estimates the position based on the integrated argue against differential latencies. It would be signals18. The flash-lag occurs because position interesting to repeat the temporal order experiment information of the flashed stimulus is hypothesized to for an object that remains in motion after the flash. persist for some time19 and therefore biases the The differential latencies hypothesis loses some of position estimate towards the last seen position of the its appeal when one considers the rich flash (Fig. 2d). phenomenology of the flash-lag effect. In a set-up with Unlike motion extrapolation, temporal averaging repetitive sequences of flashes, increasing the predicts an influence of post-flash changes on the number of flashes, the duration of the flash or the percept. The finding that reversing12 or slowing flash frequency all lead to an orderly decrease of the down15 the moving object after the flash reduces the lag3,4. Moreover, flash-lag-like phenomena not only lag, confirms this. The data diverge on the answer of apply to motion but also to other dimensions of how long after the flash the trajectory of the moving stimulus change13. In one experiment, the colour of a object still influences the lag. Some experimental spot gradually changed from green to red. At some data show a temporal horizon of about 500 ms time during the change a second spot was flashed (Ref. 3), Brenner and Smeets report 150 ms, with exactly the same colour the changing spot had at Eagleman and Sejnowski argue for an 80 ms that time. Subjects reported that the changing spot window, and Whitney et al.
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