This article describes novel attributes of the mushroom bodies of cockroaches revealed by recording from neurons in freely moving insects. The results suggest several hitherto unrecognized functions of the mushroom bodies: extrinsic neurons that discriminate between imposed and self-generated sensory stimulation, extrinsic neurons that monitor motor actions, and a third class of extrinsic neurons that predict episodes of locomotion and modulate their activity depending on the turning direction. Electrophysiological units have been correlated with neurons that were partially stained by uptake of copper ions and silver intensification. Neurons so revealed correspond to Golgi-impregnated or Lucifer yellow-filled neurons and demonstrate that their processes generally ascend to other areas of the protocerebrum. The present results support the idea of multiple roles for the mushroom bodies. These include sensory discrimination, the integration of sensory perception with motor actions, and, as described in the companion article, a role in place memory.