The habenula and interpeduncular nucleus (IPN) are part of a dorsal diencephalic conduction system which receives input from cholinergic, striatal, and hypothalamic areas, and sends output to several, disparate midbrain regions. These output regions include the dorsal tegmental nucleus, which is part of a navigation-related system that provides a signal for directional heading. The habenula and IPN also project to the dorsal and medial Raphe nuclei, thought to be involved in mood and behavioral state regulation. Here, cells in both the habenula and IPN were recorded in freely moving rats while they foraged for food pellets. There were four major findings. First, many of the cells tended to fire in sporadic bouts of relatively high versus low rates, and this may be related to intrinsic cell properties discovered during in vitro studies. Second, although these regions are connected to the direction signaling circuit, they do not, themselves demonstrate a directional signal. Third, about 10% of the cells in the lateral habenula showed a strong correlation between rate and angular head motion. This may constitute an important, requisite input to the above-mentioned head direction circuit. Finally, many of the cells in each region showed a temporally coarse correlation with running speed, so that bouts of high frequency firing coincided with episodes of higher behavioral activation. This last finding may be related to work which shows an influence of the habenula on locomotor activity, and in relation to the protective effects of exercise in relation to stress, as mediated by the Raphe nuclei.