Lesions of the tegmentomammillary circuit in the head direction system disrupt the head direction signal in the anterior thalamus

Head direction (HD) cells in the rodent limbic system are believed to correspond to a cognitive representation of directional heading in the environment. Lesions of vestibular hair cells disrupt the characteristic firing patterns of HD cells, and thus vestibular afference is a critical contributor to the HD signal. A subcortical pathway that may convey this information includes the dorsal tegmental nucleus of Gudden (DTN) and the lateral mammillary nucleus (LMN). To test the hypothesis that the DTN and LMN are critical components for generating HD cell activity, we made electrolytic lesions of the DTN or LMN in rats and screened for HD cell activity in the anterior thalamus. Directional activity was absent in all animals with complete LMN lesions and in animals with complete DTN lesions, although a few HD cells were isolated in animals with incomplete lesions. Some DTN-lesioned animals contained cells whose firing rates were modulated by angular head velocity. Although cells with bursting patterns of activity have been observed in the anterior dorsal nucleus of the thalamus of animals with disruption of vestibular inputs, this pattern of activity was not observed in either the LMN- or DTN-lesioned animals. The general absence of direction- specific activity in the anterior thalamus of animals with DTN or LMN lesions is consistent with the view that the DTN-LMN circuit is essential for the generation of HD cell activity.