TRANSITIONS BETWEEN PURSUIT EYE-MOVEMENTS AND FIXATION IN THE MONKEY - DEPENDENCE ON CONTEXT

1. We compared the visuomotor processing underlying the onset and offs et of pursuit by recording the eye movements of three monkeys as they smoothly tracked a target that was initially at rest, started to move suddenly at a constant velocity along the horizontal meridian, and the n stopped. We presented this sequence of target motions in two differe nt contexts. In the first context the target sometimes stopped after 5 00 ms, but on other interleaved trials the target either continued mov ing at a constant velocity, slowed down, speeded up, or reversed direc tion. In the second context the target always stopped, but the duratio n of the preceding constant velocity was randomized from 500 to 700 ms . 2. The dynamics of the eye velocity during the offset of pursuit wer e markedly different in the two experiments. When the target stopped o nly sometimes, the decrease in eye velocity at the offset of pursuit o ften overshot zero, producing a brief, small reversal in the direction of pursuit before eye speed settled to zero. When the target always s topped, the decrease in eye velocity at the offset of pursuit followed a more gradual transition toward zero with no overshoot. Thus the eye velocity profiles obtained in the first experiment contradict, wherea s those obtained in the second experiment confirm, previous characteri zations of the offset of pursuit as an exponential decay toward zero e ye speed. 3. To investigate the basis of the different eye velocity pr ofiles obtained in the two experiments, we probed the state of transmi ssion along the visuomotor pathways for pursuit with the use of small perturbations in the motion of the target. We used perturbations consi sting of 1 degrees step changes in target position superimposed on the constant velocity motion of the target, on the basis of previous find ings that such perturbations elicit saccades during fixation but smoot h changes in eye speed during maintained pursuit. Single perturbations were imposed at regularly spaced intervals on separate interleaved tr ials during the onset, maintenance, and offset of pursuit. 4. Perturba tions imposed during the onset and maintenance of pursuit had similar effects regardless of whether the target stopped only sometimes or alw ays. In both experiments, perturbations that stepped the target in the direction opposite to the constant velocity of the target produced de creases in eye speed; perturbations in the same direction produced neg lible or inconsistent changes in eye speed. The changes in eye speed c aused by perturbations were largest for those perturbations introduced within the first 100 ms after the start of target motion, before the onset of the smooth eye movement, and became progressively smaller as target motion continued. The largest changes in eye speed were therefo re caused by those perturbations imposed during periods of large retin al slip and by those perturbations whose direction opposed that slip. 5. Perturbations imposed during the offset of pursuit had different ef fects depending on whether the target stopped only sometimes or always . When the target stopped only sometimes, forward perturbations produc ed large increases in eye speed, whereas backward perturbations produc ed negligible or inconsistent changes in eye speed. Thus the visuomoto r processing underlying the offset of pursuit in this experiment stron gly resembled that underlying the onset of pursuit: in both cases, tho se perturbations in the direction opposing large retinal slip produced the largest effects. In contrast, when the target always stopped, nei ther forward nor backward perturbations imposed during the offset of p ursuit produced large changes in eye speed. This indicates that the vi suomotor processing underlying the offset of pursuit in this experimen t was different from the processing underlying the onset of pursuit. 6 . Perturbations also produced changes in the frequency of saccades, al though these effects were less consistent than the changes in pursuit eye speed. During the onset of pursuit, such effects as did occur were similar in the two experiments: perturbations in the same direction a s the motion of the target increased the frequency of saccades, wherea s perturbations in the opposite direction either decreased the frequen cy of saccades or had no effect. In contrast, during the offset of pur suit, perturbations had different effects on saccadic frequency, depen dent on whether the target stopped only sometimes or always. When the target stopped only sometimes, backward perturbations increased the fr equency of saccades, whereas forward perturbations decreased the frequ ency of saccades. However, when the target always stopped, there was l ittle difference between the effects of forward and backward perturbat ions on saccades. Thus the effects of the perturbations on the program ming of saccades complemented the effects on smooth eye velocity. 7. O ur data indicate that the visuomotor processing underlying the offset of pursuit can be either very similar to or very different from that u nderlying the onset of pursuit. These results raise doubts about the p revious proposal that the onset and offset of pursuit are mediated by different mechanisms. For parsimony, we suggest that the onset and off set of pursuit are mediated by a single mechanism, but that the transm ission of visual and motor signals through this mechanism can vary dur ing pursuit. We present simulations to demonstrate that a model incorp orating this suggestion can account for the variety of eye velocity pr ofiles observed during the onset and offset of pursuit.