Extra-retinal adaptation of cortical motion-processing areas during pursuit eye movements

Abstract

Repetitive eye movement produces a compelling motion aftereffect (MAE). One mechanism thought to contribute to the illusory movement is an extra-retinal motion signal generated after adaptation. However, extra-retinal signals are also generated during pursuit. They modulate activity within cortical motion-processing area MST, helping transform retinal motion into motion in the world during an eye movement. Given the evidence that MST plays a key role in generating MAE, it may also become indirectly adapted by prolonged pursuit. To differentiate between these two extra-retinal mechanisms we examined storage of the MAE across a period of darkness. In one condition observers were told to stare at a moving pattern, an instruction that induces a more reflexive type of eye movement. In another they were told to deliberately pursue it. We found equally long MAEs when testing immediately after adaptation but not when the test was delayed by 40 s. In the case of the reflexive eye movement the delay almost completely extinguished the MAE, whereas the illusory motion following pursuit remained intact. This suggests pursuit adapts cortical motion-processing areas whereas unintentional eye movement does not. A second experiment showed that cortical mechanisms cannot be the sole determinant of pursuit-induced MAE. Following oblique pursuit, we found MAE direction changes from oblique to vertical. Perceived MAE direction appears to be influenced by a subcortical mechanism as well, one based on the relative recovery rate of horizontal and vertical eye-movement processes recruited during oblique pursuit.

Figure 1

(a) Eye movements made when instructed to deliberately pursue the adapting stimulus (upper panel) or stare at it (lower panel). The histograms plot the frequency of the slow-phase durations (the time between individual saccades). (b) MAE duration following deliberate pursuit (closed symbols) or reflexive nystagmus (open symbols). Error bars are ±1 s.e.

Figure 2

(a) Sample eye-movement recordings for one observer. The left column shows the horizontal component and the right the vertical. Black traces correspond to adaptation period and red the test phase. Vertical spikes correspond to eye blinks. (b) Mean MAE durations. Error bars are +1 s.e. (c) Final MAE direction in the diagonal-adaptation conditions, plotted as a function of the ratio of MAE duration in the vertical and horizontal adaptation conditions. (d) Final MAE direction in the diagonal conditions, plotted as a function of the ratio between vertical to horizontal component eye-movement speeds during diagonal pursuit.