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J Neurophysiol 93: 1510-1522, 2005. First published October 13, 2004; doi:10.1152/jn.00543.2004
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Processing of Retinal and Extraretinal Signals for Memory-Guided Saccades During Smooth Pursuit

Gunnar Blohm1,2, Marcus Missal2 and Philippe Lefèvre1,2,3

1Centre for Systems Engineering and Applied Mechanics, Université Catholique de Louvain, Louvain-la-Neuve, Belgium; 2Laboratory of Neurophysiology, Université Catholique de Louvain, Brussels, Belgium; and 3National Eye Institute, National Institutes of Health, Bethesda, Maryland

Submitted 25 May 2004; accepted in final form 10 October 2004

It is an essential feature for the visual system to keep track of self-motion to maintain space constancy. Therefore the saccadic system uses extraretinal information about previous saccades to update the internal representation of memorized targets, an ability that has been identified in behavioral and electrophysiological studies. However, a smooth eye movement induced in the latency period of a memory-guided saccade yielded contradictory results. Indeed some studies described spatially accurate saccades, whereas others reported retinal coding of saccades. Today, it is still unclear how the saccadic system keeps track of smooth eye movements in the absence of vision. Here, we developed an original two-dimensional behavioral paradigm to further investigate how smooth eye displacements could be compensated to ensure space constancy. Human subjects were required to pursue a moving target and to orient their eyes toward the memorized position of a briefly presented second target (flash) once it appeared. The analysis of the first orientation saccade revealed a bimodal latency distribution related to two different saccade programming strategies. Short-latency (<175 ms) saccades were coded using the only available retinal information, i.e., position error. In addition to position error, longer-latency (>175 ms) saccades used extraretinal information about the smooth eye displacement during the latency period to program spatially more accurate saccades. Sensory parameters at the moment of the flash (retinal position error and eye velocity) influenced the choice between both strategies. We hypothesize that this tradeoff between speed and accuracy of the saccadic response reveals the presence of two coupled neural pathways for saccadic programming. A fast striatal-collicular pathway might only use retinal information about the flash location to program the first saccade. The slower pathway could involve the posterior parietal cortex to update the internal representation of the flash once extraretinal smooth eye displacement information becomes available to the system.


Address for reprint requests and other correspondence: P. Lefèvre, CESAME, Université Catholique de Louvain, 4, Avenue G. Lemaître, 1348 Louvain-la-Neuve, Belgium (E-mail: lefevre{at}csam.ucl.ac.be)




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