Evidence for a Retinal Velocity Memory Underlying the Direction of 9 Anticipatory Smooth Pursuit Eye Movements

37 To compute spatially correct smooth pursuit eye movements, the brain uses both retinal 38 motion and extraretinal signals about the eyes and head in space (Blohm and Lefèvre 2010). 39 However, when smooth eye movements rely solely on memorized target velocity, such as during 40 anticipatory pursuit, it is unknown if this velocity memory also accounts for extraretinal 41 information such as head roll and ocular torsion. To answer this question, we used a novel 42 behavioral updating paradigm in which participants pursued a repetitive, spatially constant 43 fixation-gap-ramp stimulus in series of five trials. During the first four trials, participants’ heads 44 were rolled towards one shoulder, inducing ocular counter-roll (OCR). With each repetition, 45 participants increased their anticipatory pursuit gain, indicating a robust encoding of velocity 46 memory. On the fifth trial, they rolled their heads to the opposite shoulder prior to pursuit, also 47 inducing changes in ocular torsion. Consequently, for spatially accurate anticipatory pursuit, the 48 velocity memory had to be updated across changes in head roll and ocular torsion. We tested 49 how the velocity memory accounted for head roll and OCR by observing the effects of changes 50 to these signals on anticipatory trajectories of the memory decoding (fifth) trials. We found that 51 anticipatory pursuit was updated for changes in head roll; however, we observed no evidence of 52 compensation for OCR, representing the absence of ocular torsion signals within the velocity 53 memory. This indicated that the directional component of the memory must be coded retinally 54 and updated to account for changes in head roll, but not OCR. 55 56