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Consistent Chronostasis Effects Across Saccade Categories Imply a Subcortical Efferent Trigger

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Consistent Chronostasis Effects Across Saccade Categories Imply a Subcortical Efferent Trigger Consistent Chronostasis Effects across Saccade Categories Imply a Subcortical Efferent Trigger Kielan Yarrow, Helen Johnson, Patrick Haggard, and John C. Rothwell Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/5/839/1758202/089892904970780.pdf by guest on 18 May 2021 Abstract & Saccadic chronostasis refers to the subjective temporal highly reflexive (peripherally cued saccades, express saccades). lengthening of the first visual stimulus perceived after an eye Chronostasis was similar in magnitude across all these con- movement, and is most commonly experienced as the ‘‘stopped ditions, despite wide variations in their neural bases. The clock’’ illusion. Other temporal illusions arising in the context illusion must therefore be triggered by a ‘‘lowest common of movement (e.g., ‘‘intentional binding’’) appear to depend denominator’’ signal common to all the conditions tested and upon the volitional nature of the preceding motor act. Here their respective neural circuits. Specifically, it is suggested that we assess chronostasis across different saccade types, ranging chronostasis is triggered by a low-level signal arising in response from highly volitional (self-timed saccades, antisaccades) to to efferent signals generated in the superior colliculus. & INTRODUCTION of active suppression degrade visual input (Ross, Mor- When subjects glance at a silently ticking clock, they rone, Goldberg, & Burr, 2001) leaving a ‘‘gap’’ in per- often initially think that the clock has stopped; then, ception, yet we have continuous awareness of the state after a short pause, the second hand begins to move of objects in the world. The brain simply assumes that again. Recently, an experimental paradigm has been the information in the postsaccadic image has remained introduced permitting the quantification of this subjec- constant throughout the saccade, providing the conti- tive lengthening of the postsaccadic stimulus, and the nuity we experience. Hence, postsaccadic events are effect has been termed ‘‘chronostasis’’ (Yarrow, Hag- antedated to just before saccadic onset. This antedating gard, Heal, Brown, & Rothwell, 2001). Observers fixated is a specific construction of the brain: When sensory a cross on one side of a monitor then made a saccade evidence suggests that this assumption is incorrect (as to a target ‘‘0’’ on the other side. Eye movement trig- when the target is perceived to have jumped), ante- gered a change of digit to a ‘‘1’’ which remained on dating does not occur and chronostasis is not observed. screen for 400–1600 msec. Subsequent digits (‘‘2’’, ‘‘3’’) Saccadic chronostasis findings have recently been remained on the screen for 1 sec each, culminating in the supplemented by reports of similar illusions arising after appearance of a ‘‘4’’. Subjects indicated whether the time reaching movements (Yarrow & Rothwell, 2003) or in they saw the ‘‘1’’ was longer or shorter than that for the the context of shifts of auditory attention (Hodinott-Hill, subsequent digits, allowing matched estimates to be Thilo, Cowey, & Walsh, 2002). Two theories have been derived. In general, subjects overestimated the time they proposed to explain chronostasis across these various had seen the saccadic target by about 120 msec. experimental situations. Hodinott-Hill et al. suggested Saccadic chronostasis depends upon eye movement. that the critical factor may be arousal, which is known to It is found following a saccade, but not during static influence time estimation (Wearden, Edwards, Fakhri, & viewing or when the counter is moved towards fixation Percival, 1998; Treisman, Faulkner, Naish, & Brogan, while the eye remains still. The effect also depends upon 1990). Arousal might increase the speed of a hypothet- the size of the preceding eye movement, with illusion ical pacemaker–accumulator internal clock (Treisman, size increasing approximately linearly with the duration 1963) and lead to overestimation of time immediately of a saccade. The illusion can be disrupted by some but after a movement. By contrast, Yarrow and Rothwell not all changes in the visual scene occurring mid sac- have argued that the illusion arises when movement cade. Specifically, when the counter is noticeably dis- produces uncertainty about the onset of a sensory event. placed the illusion disappears (Yarrow et al., 2001). They suggested that in saccadic chronostasis, the initial These data suggest the following explanation of the response of neurons with receptive fields that shift in effect. During a saccade, retinal blur and mechanisms the temporal vicinity of a movement (Umeno & Gold- berg, 1997; Walker, Fitzgibbon, & Goldberg, 1995; Du- University College London hamel, Colby, & Goldberg, 1992) may be used as a time D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:5, pp. 839–847 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892904970780 by guest on 27 September 2021 marker for the onset of perceptual properties that are together, as if they had been temporally bound. This only established later (Yarrow & Rothwell, 2003). The finding shows a striking resemblance to chronostasis, idea that a specific neural event might subsequently be where a postmovement event is antedated to the point used as a time marker for temporal judgements has a of movement initiation. A second result was that this clear precedent. It was used by Libet, Wright, Feinstein, binding effect disappeared (and was even reversed) in and Pearl (1979) to explain why trains of direct electrical the absence of volition, when transcranial magnetic stimulation of a duration just long enough to elicit tactile stimulation (TMS) was applied over the contralateral sensation (approx. 200 msec) appear delayed relative to motor cortex to elicit a movement. This led the authors stimulation of the skin if applied to the somatosensory to term their effect ‘‘intentional binding,’’ considering it cortex, but not when applied to the medial lemniscus to depend upon the volitional nature of the motor act. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/5/839/1758202/089892904970780.pdf by guest on 18 May 2021 (see Pockett, 2002, for a critique). In light of these experiments, it seems natural to ask The arousal account cannot give a satisfactory expla- whether chronostasis also depends upon volition. Vary- nation for a number of experimental results, such as the ing the self-timed/cued nature of a saccade approximates illusion’s dependency on saccade size and the spatial the manipulation of volition provided by comparing self- continuity of the saccade target. However, the alterna- timed actions with movements induced by TMS. If tive receptive-field-shift account also faces difficulties. chronostasis has a volitional origin, we might reasonably The pronounced variability across cells in the timing of predict that chronostasis will be reduced for cued sac- receptive field shifts makes this event unsuitable as a cades relative to volitional saccades. In Experiment 1, time marker (Kusunoki & Goldberg, 2003). In reformu- chronostasis was therefore measured following cued lating this account in the discussion, we will suggest that saccades made in response to a sudden and unpredict- receptive field shifts (and other processes relating more able peripheral onset (prosaccades). In addition, anti- directly to duration estimation) are triggered by a spe- saccades (saccades made in a direction opposite to a cific efference copy signal that may be generated else- sudden peripheral onset) were considered. This task where in the brain. Receptive field shifts may then requires active suppression of a dominant response, underlie conscious visual perception at the time chrono- yielding a high volitional component and slow reaction stasis occurs; subjective experience might effectively times (Hallett, 1978). In antisaccades, the intention to reflect an average of the temporally smeared represen- move should occur at a normal latency after the instruc- tation provided by a large number of neurons. tive stimulus. However, this intention is translated into The present experiments do not address the arousal an actual eye movement only after a much longer delay and receptive-field-shift hypotheses directly, but were than in prosaccades because of the substantial additional instead designed to assess the neural/cognitive level time taken to inhibit the prepotent, reflexive response at which the signal that triggers the saccadic chrono- to saccade ‘‘towards’’ the target instead of away from it. stasis illusion arises. In the original saccadic experi- It follows that the temporal interval between the time of ments, chronostasis was elicited using a ‘‘self-timed’’ intention and the time of movement onset will be saccade. However, a number of different kinds of sac- greater in the antisaccade condition than in the prosac- cade have been identified (e.g., Deubel, 1996), differing cade condition; the antisaccade condition increases the primarily along a dimension which might be termed separation between these events. A comparison be- the intentional–reactive axis. To assess whether chrono- tween pro- and antisaccades allows us to investigate stasis arises at the level of (1) volitional or (2) low-level whether the chronostasis effect is tied to the intention ocu-lomotor processes, we therefore compared the or to the movement. Specifically, if we assume that the illusion’s magnitude for various types of saccade. This signal driving chronostasis were to arise early
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