Many neurons in the rat lateral mammillary nuclei (LMN) fire selectively in relation to the animal's head direction (HD) in the horizontal plane independent of the rat's location or behavior. One hypothesis of how this representation is generated and updated is via subcortical projections from the dorsal tegmental nucleus (DTN). Here we report the type of activity in DTN neurons. The majority of cells (75%) fired as a function of the rat's angular head velocity (AHV). Cells exhibited one of two types of firing patterns: (1) symmetric, in which the firing rate was positively correlated with AHV during head turns in both directions, and (2) asymmetric, in which the firing rate was positively correlated with head turns in one direction and correlated either negatively or not at all in the opposite direction. In addition to modulation by AHV, some of the AHV cells (40.1%) were weakly modulated by the rat's linear velocity, and a smaller number were modulated by HD (11%) or head pitch (15.9%). Autocorrelation analyses indicated that with the head stationary, AHV cells displayed irregular discharge patterns. Because afferents from the DTN are the major source of information projecting to the LMN, these results suggest that AHV information from the DTN plays a significant role in generating the HD signal in LMN. A model is proposed showing how DTN AHV cells can generate and update the LMN HD cell signal.
Key words: dorsal tegmental nucleus of Gudden; lateral mammillary nuclei; head direction cell; angular head velocity; nucleus prepositus hypoglossi; directional heading; neural integration; vestibular system; navigation; spatial orientationNeurons that discharge selectively in relation to an animal's head direction (HD) in the horizontal plane (HD cells) have been identified in several limbic system structures in the rat, including the postsubiculum (Taube et al., 1990a), anterior dorsal thalamic nucleus (ADN) (Taube, 1995), lateral mammillary nuclei (LMN) (Blair et al., 1998;Stackman and Taube, 1998), lateral dorsal thalamic nucleus (Mizumori and Williams, 1993), and retrosplenial cortex (Chen et al., 1994;Cho and Sharp, 2001). These brain areas are interconnected with one another in the classic Papez circuit. A series of lesion studies has identified the sequence of processing of the HD signal. Goodridge and Taube (1997) found that lesions of the ADN disrupted HD cell firing in the postsubiculum but that lesioning the postsubiculum left HD cell firing intact in the ADN. Two recent studies have established that bilateral lesions of the LMN disrupt HD cell firing in the ADN (Tullman and Taube, 1998;Blair et al., 1999). Thus, the HD cell signal appears to be generated in the LMN or in areas afferent to it.Previous studies have postulated that the ADN serves as a convergence point for different types of spatial information onto HD cells, with idiothetic or self-generated cues about movement (e.g., vestibular, proprioceptive, and motor efference copy) ascending from subcortical structures and allothetic or externally orig...