Subpopulation of thalamic neurons possesses distinct anatomical connectivities and electrophysiological properties in the anterior thalamic nucleus

The Head Direction (HD) system is important for spatial orientation. The Anterior thalamic nucleus (ATN) is one of the critical brain regions for the system. It is composed of two main subdivisions: the anterodorsal nucleus (AD) and anteroventral nucleus (AV). It receives HD inputs originated from the lateral mammillary nucleus (LMN), and it sends HD information to the retrosplenial cortex (RSC) and presubiculum (PrS). However, it has been unclear which thalamic neurons target RSC or PrS. Moreover, the input connectivity from the upstream lateral mammillary nucleus (LMN) is has not been clearly elucidated. In this study, thalamic neurons are investigated to characterize their 1) anatomical connectivity to the cortical regions, 2) electrophysiological intrinsic properties and 3) responses to photostimulation of mammillary nucleus inputs. Our work demonstrates a topographical distribution of RSC-projecting and PrS-projecting populations of neurons in the ATN. Some ATN neurons possess bifurcating axons and project to both cortical areas. AD and AV neurons have distinct electrophysiological intrinsic properties. We find differences in time constant, input-output resistance, sag ratio, resting membrane potential, and firing patterns. This suggests that the two thalamic subdivisions might send different information to the cortical regions. Lastly, we observe short latency synaptic responses of ATN neurons following the optical stimulation of axons originating from the mammillary nuclei. The responses were variable between AD and AV. Taken together, our data provide new elements to better understand the role of the ATN in the HD system.