We demonstrate that distinct mechanisms of top-down control regulate, respectively, the sensitivity and gain of sensory responses in the owl's optic tectum (OT). Electrical microstimulation in the forebrain gaze control area, the arcopallial gaze field (AGF), results in a space-specific regulation of sensory responses in the OT. AGF microstimulation increases the responsiveness of OT neurons representing stimuli at the same location as that represented at the AGF site. We show that the mechanism that underlies this effect operates focally to enhance neuronal sensitivity and improve tuning consistency and spatial resolution. At the same time, AGF microstimulation decreases the responsiveness of OT neurons representing stimuli at all other locations. The mechanism that underlies this effect operates globally to modulate neuronal gain. The coordinated action of these different mechanisms can account for many of the reported effects of spatial attention on neural responses in monkeys and on behavioral performance in humans.