The Head Direction (HD) system is crucial for spatial orientation. The anterior thalamic nucleus (ATN) is one of its key brain regions. It is composed of two main subdivisions: the anterodorsal (AD) and the anteroventral nucleus (AV). ATN receives HD input originating from the lateral mammillary nucleus (LMN), and it sends HD information to the retrosplenial cortex (RSC) and to the presubiculum (PrS). However, it has been unclear which thalamic projecting neurons target RSC or PrS or both. In this study, anterior thalamic neurons were investigated to elucidate their 1) anatomical output connectivity to these two cortical regions, 2) electrophysiological intrinsic properties and 3) electrophysiological responses to the activation of LMN inputs. First, we demonstrate a topographical segregation and some overlap of gRSC-projecting and PrS-projecting populations of neurons in the ATN in mice. Retrograde tracers (CTB) conjugated with different fluorescent proteins were injected in gRSC and PrS, and labelled neurons in the ATN were quantified. In AD, gRSC-projecting neurons were ventro-laterally located, while PrS-projecting neurons were dorso-medially located. 38% of labelled AD neurons were doubly labelled. In AV, gRSC-projecting neurons were ventro-medially located, and PrS-projecting neurons were dorso-laterally located. 5% of the labelled AV neurons were doubly labelled. Second, we found that AD and AV neurons possess distinct electrophysiological intrinsic properties. A total of 36 neurons were recorded in acute brain slices containing the thalamus, using the whole cell patch clamp technique. Neurons in the two nuclei differed in their mean resting membrane potential (AD: -61.5 mV vs. AV: -71.8 mV), time constant (12.3 ms vs. 18.5 ms), sag ratio (1.42 vs. 1.06), input-output relation (382 Hz/nA vs. 173 Hz/nA), firing patterns (adaptive vs. irregular), and the presence or absence of a post-train hyperpolarization. This result suggests that these two thalamic nuclei differently process information sent to cortex. Lastly, AAV-Chronos was injected into the LMN. Axons originating from LMN targeted the AD and AV. The projecting fibers were strongly innervating AD and dorsal AV, and to a lesser degree the ventral AV. Initial results found short latency excitatory responses in ATN neurons following the optogentic stimulation of axons from LMN in slices. Taken together, our data provide new insight in the routing of HD information via the ATN to Presubiculum and the Retrosplenial Cortex.