Division of labor between frontal eye field neurons during spatial visual processing
SooYoon Shin and Marc A. Sommer
Some neurons in the visual system exhibit presaccadic remapping (Duhamel et al. 1992): just before a saccadic eye movement, they become less active at their receptive field (RF) and more active at a new location, their future field (FF). The FF is the location where the RF will settle just after the saccade ends. Such neurons therefore sample the same part of absolute visual space before and after a saccade, which may contribute to our percept of visual stability as we look around. For remapping to occur, a neuron needs to know where the eyes are going, and such advanced information about saccades is provided by the superior colliculus (Sommer & Wurtz 2006). The collicular information is relayed by the thalamus to layer IV of the frontal eye field. Here we asked what happens in layer IV. Do the layer IV neurons show "full" presaccadic remapping (decreased RF activity plus increased FF activity), partial remapping (e.g. decreased RF activity but no change in FF activity), or no remapping at all? We identified layer IV neurons in frontal eye field by orthodromically activating them from the superior colliculus, we mapped their RFs and FFs, and we recorded their action potential waveforms. Critically, we compared the waveforms to a calibration set from known pyramidal neurons (frontal eye field neurons antidromically activated from the superior colliculus). We found three types of layer IV neurons. Putative excitatory neurons (indistinguishable from pyramidal neurons) showed partial remapping: a decrease in RF activity but no change in FF activity. Putative inhibitory neurons (narrower waveforms than pyramidal neurons) showed no remapping. A third, intermediate class showed no change in RF activity but an increase in FF activity. If the signals of the first and third classes were combined, they would produce full remapping (decreased RF activity plus increased FF activity). We conclude that layer IV neurons in the frontal eye field exhibit a division of labor. They do not accomplish the complex phenomenon of presaccadic remapping in a single step; rather, they create the necessary component signals and then route them downstream for assembly.
