Chronic motor learning in the vestibulo-ocular reflex (VOR) results in changes in the gain of this reflex and in other eye movements associated with VOR behavior, e.g., the velocity storage generated by optokinetic stimulation (OKN velocity storage). The aim of the present study was to identify the plastic sites responsible for the change in OKN velocity storage following chronic VOR motor learning. We studied the responses of vertical eye movement flocculus target neurons (FTNs) during the optokinetic afternystagmus (OKAN) phase of the optokinetic response before and after VOR motor learning. Our findings can be summarized as follows: i) chronic VOR motor learning changes the horizontal OKN velocity storage in parallel with changes in VOR gain, while the vertical OKN velocity storage is more complex, increasing with VOR gain increases, but not changing following VOR gain decreases. ii) FTNs response during OKAN has opposite directional preferences after chronic high versus low gain learning; iii) Changes in the eye velocity sensitivity of FTNs during OKAN are correlated with changes in their brainstem head velocity sensitivity; and iv) These changes in eye velocity sensitivity of FTNs during OKAN support the new behavior after high gain but not low gain learning. Thus we hypothesize that the changes observed in the OKN velocity storage behavior after chronic learning result from changes in brainstem pathways carrying head velocity and OKN velocity storage information, and that a parallel pathway to vertical FTNs changes its OKN velocity storage representation following low, but not high, gain VOR motor learning.