Generating the head direction signal: Two types of head direction cells in the lateral mammillary and dorsal tegmental nuclei.

Abstract

Head direction (HD) cells discharge as a function of the animals directional heading and are believed to underlie ones sense of direction. They have been identified in several brain areas, although the signal is thought to be generated across the connections between the lateral mammillary (LMN) and dorsal tegmental nuclei (DTN). Computational models have proposed that a ring-attractor network underlies the mechanisms that generate the signal. These models usually contain separate populations of neurons that encode HD and angular head velocity (AHV). Currently, both cell types have been identified in the LMN and DTN. However, HD attractor models also require cells, referred to as rotation cells, which are sensitive to both parameters conjunctively (HD+AHV). Here we sought to identify such cells in the LMN-DTN network. We identified two distinct types of HD cells. The majority of LMN HD cells ([~]64%) were AHV-independent, responding only to the animals directional heading. However, a second population ([~]36%) was sensitive to both HD and AHV. Both symmetric and asymmetric AHV cell types were found. Similar results were found in the DTN, but with a higher percentage of conjunctive HD+AHV cells (60%). Notably, many HD+AHV conjunctive cells were also sensitive to the animals linear velocity (LV). In contrast, HD cells in the anterodorsal thalamus were rarely sensitive to AHV or LV. These findings demonstrate that the requisite rotation-type HD cell is present in brain areas responsible for generating the HD signal and supports the view that an attractor style network underlies its generation in mammals. Statements and DeclaratioThis manuscript does not represent the official view of the National Institute of Neurological Disorders and Stroke (USA) (NINDS), the National Institutes of Health (USA) (NIH), or any part of the US Federal Government. No official support or endorsement of this article by the NINDS or NIH is intended or should be inferred.