Intact landmark control and angular path integration by head direction cells in the anterodorsal thalamus after lesions of the medial entorhinal cortex

Abstract

The medial entorhinal cortex (MEC) occupies a central position within neural circuits devoted to the representation of spatial location and orientation. The MEC contains cells that fire as a function of the animal's head direction (HD), as well as grid cells that fire in multiple locations in an environment, forming a repeating hexagonal pattern. The MEC receives inputs from widespread areas of the cortical mantle including the ventral visual stream, which processes object recognition information, as well as information about visual landmarks. The role of the MEC in processing the HD signal or landmark information is unclear. We addressed this issue by neurotoxically damaging the MEC and recording HD cells within the anterodorsal thalamus (ADN). Direction-specific activity was present in the ADN of all animals with MEC lesions. Moreover, the discharge characteristics of ADN HD cells were only mildly affected by MEC lesions, with HD cells exhibiting greater anticipation of future HDs. Tests of landmark control revealed that HD cells in lesioned rats were capable of accurately updating their preferred firing directions in relation to a salient visual cue. Furthermore, cells from lesioned animals maintained stable preferred firing directions when locomoting in darkness and demonstrated stable HD cell tuning when locomoting into a novel enclosure, suggesting that MEC lesions did not disrupt the integration of idiothetic cues, or angular path integration, by HD cells. Collectively, these findings suggest that the MEC plays a limited role in the formation and spatial updating of the HD cell signal.