Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity

A new approach was developed to investigate the role of visual-, movement-, and fixation-related neural activity in gaze control. We recorded unit activity in the frontal eye fields (FEF), an area in frontal cortex that plays a central role in the production of purposeful eye movements, of monkeys (Macaca mulatta) performing visually and memory-guided saccades. The countermanding paradigm was employed to assess whether single cells generate signals sufficient to control movement production. The countermanding paradigm consists of a task that manipulates the monkeys' ability to withhold planned saccades combined with an analysis based on a race model that provides an estimate of the time needed to cancel the movement that is being prepared. We obtained clear evidence that FEF neurons with eye movement-related activity generate signals sufficient to control the production of gaze shifts. Movement-related activity, which was growing toward a trigger threshold as the saccades were prepared, decayed in response to the stop signal within the time required to cancel the saccade. Neurons with fixation-related activity were less common, but during the countermanding paradigm, these neurons exhibited an equally clear gaze-control signal. Fixation cells that had a pause in firing before a saccade exhibited elevated activity in response to the stop signal within the time that the saccade was cancelled. In contrast to cells with movement or fixation activity, neurons with only visually evoked activity exhibited no evidence of signals sufficient to control the production of gaze shifts. However, a fraction of tonic visual cells exhibited a reduction of activity once a saccade command had been cancelled even though the visual target was still present in the receptive field. These findings demonstrate the use of the countermanding paradigm in identifying neural signatures of motor control and provide new information about the fine balance between gaze shifting and gaze holding mechanisms.