How Do Primates Anticipate Uncertain Future Events?

In motor control, prediction of future events is vital for overcoming sensory-motor processing delays and facilitating rapid and accurate responses in a dynamic environment. In human ocular pursuit this is so pervasive that prediction of future target motion cannot easily be eliminated by randomizing stimulus parameters. We investigated the prediction of temporally randomized events during pursuit of alternating constant-velocity (ramp) stimuli in which the timing of direction changes varied unpredictably over a given range. Responses were not reactive; instead, smooth eye velocity began to decelerate in anticipation of each target reversal. In the first experiment, using a continuous-motion stimulus, we found that the time at which this occurred was relatively constant regardless of ramp duration, but increased as mean ramp duration of the range increased. Regression analysis revealed a quantitative association between deceleration timing and the previous two or three ramp durations in a trial, suggesting that recent stimulus history was used to create a running average of anticipatory timing. In the second experiment, we used discrete motion stimuli, with intervening periods of fixation, which allowed both target velocity and reversal timing to be varied, thereby decoupling ramp duration and displacement. This enabled us to confirm that the timing of anticipatory deceleration was based on the history of timing, rather than displacement, within the stimulus. We conclude that this strategy is used to minimize error amid temporal uncertainty, while simultaneously overcoming inherent delays in visuomotor processing.

Section: Discussionmentioning

confidence: 49%

“…This would not be surprising. Previously, when examining anticipatory responses to the onset of discrete pursuit stimuli, de Hemptinne et al (2007) showed that variability in cue timing is reflected in variability in response timing. Similar effects have been reported for saccades (Joiner and Shelhamer, 2006).…”

Section: Discussionmentioning

confidence: 99%

Predicting the Unpredictable: Weighted Averaging of Past Stimulus Timing Facilitates Ocular Pursuit of Randomly Timed Stimuli

Collins¹,

Barnes²

2009

“…Therefore, the latency distribution of anticipatory pursuits is bimodal (Fig. 5A2,B2) (see also de Hemptinne et al, 2006de Hemptinne et al, , 2007. Figure 9 shows that the cumulative latency distribution of anticipatory pursuit movements shows two abrupt increases (onset indicated by vertical dashed lines; see also aЈ and bЈ).…”

Section: Modulation Of Neuronal Activity Related To Anticipatory Pursuitmentioning

confidence: 89%

“…Anticipatory smooth pursuit is a slow movement of the eyes occurring before the appearance of an expected moving target. It has been shown repeatedly that primates can generate anticipatory smooth pursuit in the absence of visual stimulation provided there is a strong expectation about the characteristics of upcoming target motion (Kowler andSteinman, 1979a,b, 1981;Kowler et al, 1984;Kowler, 1989;Barnes and Asselman, 1991;Barnes et al, 2002;Heinen et al, 2005;Badler and Heinen, 2006;de Hemptinne et al, 2007). The influence of expectation in the spatial domain is often studied by providing information using color cues that allow subjects to orient attention to the upcoming spatial position of a target (Posner, 1980).…”

Section: Introductionmentioning

confidence: 99%

Neuronal Bases of Directional Expectation and Anticipatory Pursuit

Hemptinne¹,

Lefèvre²,

Missal³

2008

Self Cite

Expectation of upcoming events is an essential cognitive function on which anticipatory actions are based. The neuronal basis of this prospective representation is poorly understood. We trained rhesus monkeys in a smooth-pursuit task in which the direction of upcoming target motion was indicated using a color cue. Under these conditions, directional expectation frequently evoked anticipatory smooth movements. We found that the activity of a population of neurons in the supplementary eye fields encoded the expected future direction of the target. Neuronal activity increased after presentation of the cue, indicating future target motion in the preferred direction. Neuronal activity either remained unaltered or was reduced if the antipreferred direction was cued. In addition, ϳ30% of these neurons were more active during trials with anticipatory pursuit in the preferred direction than during trials when monkeys did not anticipate target motion onset. This subset of recorded neurons encoded the direction of the subsequent anticipatory pursuit. We hypothesize that the neural representation of directional expectation could be conceptualized as a competitive interaction between pools of neurons representing likely future events, with the winner of this competition determining the direction of the subsequent anticipatory movement. Similar mechanisms could drive prediction before movement initiation in other motor domains.

“…Only saccades that occurred after the onset of launcher target motion were recorded. Pursuit onset was also detected using a previous algorithm (de Hemptinne et al, 2007). Filtered velocity was required to exceed a threshold of 2°/s for at least 100 ms to be classified as pursuit.…”

Section: Methodsmentioning

confidence: 99%

Causality Attribution Biases Oculomotor Responses

Badler

Lefèvre²,

Missal³

2010

Self Cite

When viewing one object move after being struck by another, humans perceive that the action of the first object "caused" the motion of the second, not that the two events occurred independently. Although established as a perceptual and linguistic concept, it is not yet known whether the notion of causality exists as a fundamental, preattentional "Gestalt" that can influence predictive motor processes. Therefore, eye movements of human observers were measured while viewing a display in which a launcher impacted a tool to trigger the motion of a second "reaction" target. The reaction target could move either in the direction predicted by transfer of momentum after the collision ("causal") or in a different direction ("noncausal"), with equal probability. Control trials were also performed with identical target motion, either with a 100 ms time delay between the collision and reactive motion, or without the interposed tool. Subjects made significantly more predictive movements (smooth pursuit and saccades) in the causal direction during standard trials, and smooth pursuit latencies were also shorter overall. These trends were reduced or absent in control trials. In addition, pursuit latencies in the noncausal direction were longer during standard trials than during control trials. The results show that causal context has a strong influence on predictive movements.