Predictive Smooth Pursuit Eye Movements

Kowler, Eileen; Rubinstein, Jason; Santos, Elio M.; Wang, Jie

doi:10.1146/annurev-vision-091718-014901

Cited by 59 publications

(46 citation statements)

References 147 publications

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“…They rely on the integration of current motion information with priors based on experience across just a few trials or across a longer-term context (Darlington et al 2017; Deravet et al 2018; Yang et al 2012). Moreover, smooth pursuit can be triggered by the expectation of a certain motion direction even before the object’s motion onset, a phenomenon known as anticipatory smooth pursuit (Kowler et al 1984, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Previous research has revealed highly consistent effects of expectation on pursuit but contrasting effects on motion perception. For example, anticipatory pursuit can be triggered when observers repeatedly view stimuli moving into the same direction (Kowler 1989; Kowler et al 2019). The eyes are then attracted to the expected motion direction prior to the onset of the stimulus (attraction bias in direction).…”

Section: Introductionmentioning

confidence: 99%

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Expectations about motion direction affect perception and anticipatory smooth pursuit differently

Rothwell

Spering

et al. 2020

Preprint

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Smooth pursuit eye movements and visual motion perception rely on the integration of current sensory signals with past experience. Experience shapes our expectation of current visual events and can drive eye movement responses made in anticipation of a target, such as anticipatory pursuit. Previous research revealed consistent effects of expectation on anticipatory pursuit-eye movements follow the expected target direction or speed-and contrasting effects on motion perception, but most studies considered either eye movement or perceptual responses. The current study directly compared effects of direction expectation on perception and anticipatory pursuit within the same direction discrimination task to investigate whether both types of responses are affected similarly or differently. Observers (n = 10) viewed high-coherence random-dot kinematograms (RDKs) moving rightward and leftward with a probability of 50, 70, or 90% in a given block of trials to build up an expectation of motion direction. They were asked to judge motion direction of interleaved low-coherence RDKs (0-15%). Perceptual judgements were compared to changes in anticipatory pursuit eye movements as a function of probability. Results show that anticipatory pursuit velocity scaled with probability and followed direction expectation (attraction bias), whereas perceptual judgments were biased opposite to direction expectation (repulsion bias). Control experiments suggest that the repulsion bias in perception was not caused by retinal slip induced by anticipatory pursuit, or by motion adaptation. We conclude that direction expectation can be processed differently for perception and anticipatory pursuit.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Expectations about motion direction affect perception and anticipatory smooth pursuit differently

Rothwell

Spering

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…First, its buildup is relatively fast, such that only a few trials are sufficient to observe the effects of specific regularities in the properties of visual motion, such as speed, timing or direction [10,44,46]. Second, it is a robust phenomenon, which has been observed on a large population of human participants and even in non-human primates (for a recent review see [47]). Note also, that human participants seem to be largely unaware of this behavior (as inferred from informal questioning).…”

Section: Plos Computational Biologymentioning

confidence: 99%

Humans adapt their anticipatory eye movements to the volatility of visual motion properties

2020

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Animal behavior constantly adapts to changes, for example when the statistical properties of the environment change unexpectedly. For an agent that interacts with this volatile setting, it is important to react accurately and as quickly as possible. It has already been shown that when a random sequence of motion ramps of a visual target is biased to one direction (e.g. right or left), human observers adapt their eye movements to accurately anticipate the target's expected direction. Here, we prove that this ability extends to a volatile environment where the probability bias could change at random switching times. In addition, we also recorded the explicit prediction of the next outcome as reported by observers using a rating scale. Both results were compared to the estimates of a probabilistic agent that is optimal in relation to the assumed generative model. Compared to the classical leaky integrator model, we found a better match between our probabilistic agent and the behavioral responses, both for the anticipatory eye movements and the explicit task. Furthermore, by controlling the level of preference between exploitation and exploration in the model, we were able to fit for each individual's experimental dataset the most likely level of volatility and analyze inter-individual variability across participants. These results prove that in such an unstable environment, human observers can still represent an internal belief about the environmental contingencies, and use this representation both for sensory-motor control and for explicit judgments. This work offers an innovative approach to more generically test the diversity of human cognitive abilities in uncertain and dynamic environments.

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“…We now test this idea on our population of FEF SEM neurons. A priori, such a mechanism could generalize to the smooth pursuit eye movement system, especially since humans and monkeys can initiate smooth pursuit in the absence of visual motion under certain conditions (Freyberg and Ilg, 2008; de Hemptinne et al, 2006; Kowler et al, 2019). Even if the output of FEF SEM truly is used as a gain signal, noise immunity might be enhanced if population activity resided in an output null state until there is a believable visual motion signal to drive pursuit initiation.…”

Section: Resultsmentioning

confidence: 99%

Mechanisms that allow cortical preparatory activity without inappropriate movement

Darlington

Lisberger

2019

Preprint

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32We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related 33 cortical areas without prematurely inducing movement. The smooth eye movement region of the 34 frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye 35 movement. Preparatory activity evolves in FEFSEM during fixation in parallel with an objective 36 measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal 37 allows for preparation to progress in the pursuit system without causing movement. We also 38 show that preparatory modulation of firing rate in FEFSEM progresses in a way that predicts 39 movement, providing evidence against the "movement-null" space hypothesis of how 40 preparatory activity can progress without movement. Finally, there is partial reorganization of 41 FEFSEM population activity between preparation and movement. We propose that this 42 reorganization allows for a directionally non-specific component of preparatory visual-motor 43 gain enhancement in the pursuit system. 44 83of an all-or-none inhibitory gate created by the action of omnipause neurons in the brainstem 84 (Cohen and Henn, 1972; Keller, 1974a; Luschei and Fuchs, 1972). Ramps of preparatory activity 85 in the saccadic region of the frontal eye fields fail to trigger eye movements until the collective 86 descending activity from the frontal eye fields and superior colliculus cause the omnipause 87 4 neurons to cease firing, releasing the circuits that generate movement (Dorris et al., 1997; Hanes 88 and Schall, 1996). However, there is no evidence that pursuit system uses the all-or-none gate 89 that controls saccades (Missal and Keller, 2002; Schwartz and Lisberger, 1994). 90Here we propose a third, different, mechanism for movement prevention during motor 91 preparation. The outputs from the FEFSEM seem to control the gain of visual-motor transmission 92 for pursuit (Nuding et al., 2009; Tanaka and Lisberger, 2001). Further, visual-motor gain is 93 dialed up in preparation for an imminent smooth eye movement (Kodaka and Kawano, 2003; 94 Tabata et al., 2006). In the present paper, we show striking parallels between the progression of 95 preparatory activity in FEFSEM and the preparatory enhancement of visual-motor gain in the 96 pursuit system. We argue that the output of FEFSEM dials up visual-motor gain in preparation for 97 a behaviorally-relevant visual motion of a specific direction and speed, and that the use of 98 FEFSEM output as a sensorimotor gain signal allows preparation to proceed without causing 99 movement. We also show that preparatory activity in FEFSEM contradicts the predictions of the 100 dynamical system framework that has arisen from work in arm motor cortex (Churchland et al., 101 2010; Elsayed et al., 2016; Kaufman et al., 2014).102 103 Results 104Here, we present three primary findings to support the conclusion that FEFSEM preparatory 105 activity can evolve without causing smooth pursuit eye movement because its output d...

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Predictive Smooth Pursuit Eye Movements

Cited by 59 publications

References 147 publications

Expectations about motion direction affect perception and anticipatory smooth pursuit differently

Expectations about motion direction affect perception and anticipatory smooth pursuit differently

Humans adapt their anticipatory eye movements to the volatility of visual motion properties

Mechanisms that allow cortical preparatory activity without inappropriate movement

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