Characterization of prediction in the primate visual smooth pursuit system

doi:10.1016/0303-2647(94)01446-E

Biosystems

Volume 34, Issues 1–3, 1995, Pages 107-128

https://doi.org/10.1016/0303-2647(94)01446-E Get rights and content

Abstract

To define predictive behavior and mechanisms in visual smooth pursuit, various target motions were presented to 2 monkeys. Target stimuli included: single sinusoids (1′s), triangle waves (T's), sums of 4 nonharmonically related sinusoids (4′s), bandpass limited white noise (B's), and wideband white noise (N′s). Velocity error was least for 1′s, greatest for N′s, and intermediate for T's, 4′s, and B's. For the bandlimited 4′s and B's, monkeys demonstrated the greatest relative amplitude response at the highest frequencies. Predictive mechanisms are classified as short- and long-term, depending on how much past target motion information is employed. The T's and a modification of this stimulus pattern involving a random perturbation were used to test the hypothesis that prediction is based exclusively on short-term signal processing related to target position and its derivatives. The existence of long-term predictive mechanisms in monkey smooth pursuit was unequivocally demonstrated with the use of the latter stimulus.

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Because of the visuomotor delays, the ability to generate eye movements which are locked onto the current target location is obviously not possible unless the upcoming trajectory is already known. Several studies have shown that the velocity of slow eye movements hardly match the target speed when an unpredictable target is being tracked (e.g., Bahill et al., 1980; Barnes and Collins, 2015; Deno et al., 1995; Miall et al., 1986; Michael and Melvill-Jones, 1966; Mrotek et al., 2006; St-Cyr and Fender, 1969). The presence of numerous catch-up saccades makes the tracking look intermittent.
In primates, the appearance of an object moving in the peripheral visual field elicits an interceptive saccade that brings the target image onto the foveae. This foveation is then maintained more or less efficiently by slow pursuit eye movements and subsequent catch-up saccades. Sometimes, the tracking is such that the gaze direction looks spatiotemporally locked onto the moving object. Such a spatial synchronism is quite spectacular when one considers that the target-related signals are transmitted to the motor neurons through multiple parallel channels connecting separate neural populations with different conduction speeds and delays. Because of the delays between the changes of retinal activity and the changes of extraocular muscle tension, the maintenance of the target image onto the fovea cannot be driven by the current retinal signals as they correspond to past positions of the target. Yet, the spatiotemporal coincidence observed during pursuit suggests that the oculomotor system is driven by a command estimating continuously the current location of the target, i.e., where it is here and now. This inference is also supported by experimental perturbation studies: when the trajectory of an interceptive saccade is experimentally perturbed, a correction saccade is produced in flight or after a short delay, and brings the gaze next to the location where unperturbed saccades would have landed at about the same time, in the absence of visual feedback. In this chapter, we explain how such correction can be supported by previous visual signals without assuming “predictive” signals encoding future target locations. We also describe the basic neural processes which gradually yield the synchronization of eye movements with the target motion. When the process fails, the gaze is driven by signals related to past locations of the target, not by estimates to its upcoming locations, and a catch-up is made to reinitiate the synchronization.
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In terms of modelling, we have also shown that it is possible to use empirical data to inform (invert) relatively sophisticated Bayesian or normative models of behaviour. There are many carefully constructed and validated descriptive SPEM models in the literature (e.g. Barnes, 2008; Deno et al., 1995; Krauzlis and Lisberger, 1989; Krauzlis, 2004; Lisberger, 2010; Robinson et al., 1986; Shibata et al., 2005): however, the generative model that we used is distinguished in the sense that it is a special case of generic (predictive coding) models that conform to normative (Bayesian) principles. We have previously shown that formally similar generative models can reproduce both control and schizophrenic subjects’ pursuit of targets whose occlusion is either expected or unexpected, and of targets that unpredictably change direction (Adams et al., 2012).
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We show that on average, subjects respond to an increase in the ‘noise’ of target motion by increasing sensory precision in their models of the target trajectory. In other words, they attend more to the sensory attributes of a noisier stimulus. Conversely, subjects only change kinetic parameters in their model but not precision, in response to increased target speed.
Using this technique one can estimate the precisions of subjects’ hierarchical Bayesian beliefs about target motion. We hope to apply this paradigm to subjects with schizophrenia, whose pursuit abnormalities may result from the abnormal encoding of precision.
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Ocular pursuit movements allow moving objects to be tracked with a combination of smooth movements and saccades. The principal objective is to maintain smooth eye velocity close to object velocity, thus minimising retinal image motion and maintaining acuity. Saccadic movements serve to realign the image if it falls outside the fovea, the area of highest acuity. Pursuit movements are often portrayed as voluntary but their basis lies in processes that sense retinal motion and can induce eye movements without active participation. The factor distinguishing pursuit from such reflexive movements is the ability to select and track a single object when presented with multiple stimuli. The selective process requires attention, which appears to raise the gain for the selected object and/or suppress that associated with other stimuli, the resulting competition often reducing pursuit velocity. Although pursuit is essentially a feedback process, delays in motion processing create problems of stability and speed of response. This is countered by predictive processes, probably operating through internal efference copy (extra-retinal) mechanisms using short-term memory to store velocity and timing information from prior stimulation. In response to constant velocity motion, the initial response is visually driven, but extra-retinal mechanisms rapidly take over and sustain pursuit. The same extra-retinal mechanisms may also be responsible for generating anticipatory smooth pursuit movements when past experience creates expectancy of impending object motion. Similar, but more complex, processes appear to operate during periodic pursuit, where partial trajectory information is stored and released in anticipation of expected future motion, thus minimising phase errors associated with motion processing delays.
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Characterization of prediction in the primate visual smooth pursuit system

Abstract

Vision Res.

Vision Res.

Neurosci. Res.

Vision Res.

Vision Res.

Neurosci.

Vision Res.

Vision Res.

Vision Res.

Smooth pursuit eye movements in response to predictable target motions

Vision Res.

Model emulates human smooth pursuit system producing zero-latency target tracking

Biol. Cybern.

Predictive velocity estimation in the pursuit reflex response to pseudorandom and step displacement stimuli in man

J. Physiol. (Lond.)

Prediction in the oculomotor system: smooth pursuit during transient disappearance of a visual target

Exp. Brain Res.

Human smooth pursuit: stimulus-dependent responses

J. Neurophysiol.

Modern Spectral Analysis

Visual and oculomotor signals in nucleus reticularis tegmenti pontis in alert monkey

J. Neurophysiol.

Learning behavior of the eye fixation control system

IEEE Trans. on Auto. Cont.

Control theoretic investigations of the visual smooth pursuit system

Optic nystagmus III. Characteristics of the slow phase

Arch. Neurol. Psychiat.

Pursuit eye movements and their neural control in the monkey

Pflugers Arch.

Techniques of systems-analysis applied to feedback pathways in the control of eye movements

An investigation of the mechanisms of eye movement control

Kybernetik

The predictive control of behavior: appropriate and inappropriate and inappropriate actions beyond the input in a tracking task

Ergonomics