The mechanism of prediction in human smooth pursuit eye movements.

Abstract

1. Experiments have been conducted on human subjects to determine the role of prediction in smooth eye movement control. Subjects were required to actively pursue a small target or stare passively at a larger display as it moved in the horizontal plane. 2. Target motion was basically periodic, but, after a random number of cycles an unexpected change was made in the amplitude, direction or frequency of target motion. Initially, the periodic stimulus took the form of a square waveform. In subsequent experiments, a triangular or sawtooth waveform was used, but in order to examine the timing of the response in relation to stimulus appearance, the target was tachistoscopically illuminated for 40‐320 ms at the time that it passed through the mid‐line position. 3. When subjects either actively pursued the target or stared passively at the larger display a characteristic pattern of steady‐state eye movement was evoked composed of two phases, an initial build‐up of eye velocity that reached a peak after 200 ms, followed by a decay phase with a time constant of 0.5‐2 s. The build‐up phase was initiated prior to target displacement for square‐wave motion and before onset of target illumination for other waveforms. 4. The peak eye velocity evoked gradually increased over the first two to four cycles of repeated stimulation. Simultaneously, the response became more phase advanced, the reaction time between stimulus onset and the time at which peak velocity occurred decreasing from an average of 300 to 200 ms for triangular waveform stimuli. 5. When there was a sudden and unexpected change in amplitude and direction of the stimulus waveform, the eye movement induced had a peak velocity and direction that was inappropriate for the current visual stimulus, but which was highly correlated with the features of the preceding sequence in the stimulus. 6. When there was a sudden change in the frequency of the stimulus waveform the predictive eye movement was induced with a timing appropriate to the periodicity of the previous sequence but inappropriate to the new sequence. 7. The results indicate that prediction is carried out through the storage of information about both the magnitude and timing of eye velocity. The trajectory of the averaged eye velocity response was similar in form irrespective of the duration of target exposure or basic stimulus frequency, suggesting that the predictive estimate is released as a stereotyped volley of constant duration but varying magnitude under the control of a periodicity estimator.(ABSTRACT TRUNCATED AT 400 WORDS)

The contribution of the right supra-marginal gyrus to sequence learning in eye movements

“…Previous work on sequence learning has suggested that the anticipatory advantage of predictive eye movements is based upon the short-term storage of a pre-motor instruction set required for that eye movement (pursuit: Barnes & Asselman, 1991;Barnes & Donelan, 1999. saccades: Walker & McSorley, 2006Burke & Barnes, 2008a;Collins & Wallman, 2012).…”

“…Saccadic latency decreases with sequence repetition and the eye movements can even occur in advance of the onset of a new fixation stimulus (Gaymard, Pierrot-Deseilligny & Rivaud, 1990;Petit, Clark & Ingeholm, 1996;Schmid, Rees, Frith & Barnes, 2001;Barnes & Schmid, 2002;Simo, Krisky & Sweeney, 2005;Burke & Barnes 2007). In making these eye movements, observers can in effect anticipate future target locations based upon the spatial and temporal information pertaining to that specific sequence retained by memory mechanisms (Carpenter, 1988;Barnes & Asselman 1991).…”

“…The human motor system is extra-ordinarily adept at acquiring new skills and has developed sophisticated systems for the encoding and storage of spatial and temporal information that facilitate the coordinated and rapid performance of complex motor tasks (Barnes & Asselman, 1991;Kao & Morrow, 1994;Kowler & Steiman, 1979). This acquisition is accompanied by increased efficiencies in visuo-spatial processing, motor planning and motor execution (Gobel, Parrish & Reber, 2011).…”

The involvement of the fronto-parietal brain network in oculomotor sequence learning using fMRI

“…Predictive estimations are internally generated and utilized in skilled behaviour to minimise error and decrease processing delays in the sensorimotor system. Both saccadic and pursuit eye movements exhibit this predictive behaviour during repeated stimulus presentations involving the use of short-term memory storage (Barnes & Asselman, 1991) and much is now known about the mechanisms that guide these behaviours (for pursuit, see Barnes & Asselman, 1991;Missal & Heinen, 2004;Schmid, Rees, Frith, & Barnes, 2001; for saccades, see Lu, Matsuzawa, & Hikosaka, 2002). In addition, there is now substantial evidence of some commonalities in the neural networks between these two eye movement types (Krauzlis, 2005;Nyffeler, Rivaud-Pechoux, Wattiez, & Gaymard, 2008;Orban de Xivry & Lefèvre, 2007).…”

“…Indeed, there are inherent differences between the two eye movement types, in that pursuit eye movements normally rely on error correction obtained from stimulus feedback (Barnes & Asselman, 1991), whilst saccades are considered ballistic movements and can be initiated in the absence of a visual stimulus (Leigh & Zee, 1991). Furthermore, prediction in pursuit is observed after previously sampling the stimulus or cueing (Barnes & Asselman, 1991;Barnes & Donelan, 1999;Becker & Fuchs, 1985); whilst prediction in saccades can occur without this previous sampling, but wrong predictions are associated with certain costs (i.e., accuracy and timing). Thus, investigations into the learning mechanisms of these two systems will provide further insight into how the central nervous system combines different modes of motor control to achieve a common goal.…”