Inactivation of macaque lateral intraparietal area delays initiation of the second saccade predominantly from contralesional eye positions in a double-saccade task

Previous studies have shown that, although lateral intraparietal (LIP) area neurons have retinotopic receptive fields, the response strength of these cells is modulated by eye position. This combining of retinal and eye position information can form a distributed coding of target locations in a head-centered coordinate frame. Such an implicit head-centered coding offers one mechanism for maintaining spatial stability across eye movements and can be used to compute new oculomotor error vectors after each eye movement. An alternative mechanism is to use eye displacement signals rather than eye position signals to maintain spatial stability. The aim of this study was to distinguish which of these two extraretinal signals (or perhaps both signals) are employed in a double saccade task, which required the monkey to use extraretinal information associated with the first saccade to localize a remembered target for a second saccade. By varying the direction and the end point of the first saccade and selectively inactivating area LIP in one hemisphere with muscimol injection, we were able to distinguish between the two mechanisms by observing how the second saccade was impaired in this task. The displacement mechanism predicts that, if the first saccade is in the contralesional direction, the second saccade will be impaired, and the end point of the first saccade would not be important. The eye position mechanism predicts that if the first saccade ended in the contralesional head-centered space, the second saccade will be impaired, no matter in which direction the first saccade is made. Results showed that, after area LIP lesion, when the first saccade stepped into the contralesional field, the error rate of the second saccade became higher and the latency longer. However, when the end point of the first saccade was constant, the direction of the first saccade had much less effect on the second saccade. These results suggest that eye position, and not eye displacement, is the more predominant factor in this task. In a different behavioral paradigm, the monkeys performed single visual and memory saccades from different initial eye positions. It was found that the impairment of either the metrics or dynamics of visual and memory saccades did not significantly vary with the different eye positions. It thus appears that the performance of single visual and memory saccades is best described in an oculocentric coordinate frame that does not rely on extraretinal signals. Altogether these results lend further support to the hypothesis that, by combining retinal and eye position signals, area LIP contains concurrent eye-centered and head-centered representations of the visual space. Depending on the task, either representation can be used.