Dissociation between perception and predictive oculomotor behavior in retrained cortically blind fields

Abstract

When saccading to a moving peripheral target, smooth pursuit can track the target immediately upon saccade landing, reflecting pre-saccadic motion integration (Gardner and Lisberger, 2001). Similarly, saccades to peripheral, static apertures containing global motion stimuli drive predictive smooth eye movements, called “post-saccadic following responses” (PFR), along the target motion direction immediately following saccade landing (Kwon et al., 2019). PFR persists even when motion disappears in-saccade-flight, indicating that pre-saccadic motion selection initiated the subsequent following response. Here, we asked if this automatic processing persists in 7 cortically blind (CB) patients who sustained V1 damage in adulthood. Patients exhibited normal PFR gain in intact portions of their visual field (0.15±0.08), and the magnitude of PFR gain was negatively correlated with direction integration thresholds (r=−0.54, p=0.01). However, at blind field locations where patients failed to discriminate global motion direction, they exhibited no significant PFR (gain=0.004±0.019). We then asked whether visual training that recovers global motion perception in CB fields (Huxlin et al., 2009), can restore this automatic pre-saccadic processing. The resulting PFR gain was only 0.03±0.09 (t-test: p=0.6104 relative to untrained locations), well below normal (t-test: p=0.03). In summary, peripheral visual discrimination training, which recovers global motion perception in the blind field, does not restore a normal PFR. Such poor automatic pre-processing of motion in retrained CB fields suggests that after V1 damage, neural circuits engaged in the PFR may differ from those mediating conscious motion perception at the same visual field locations.