Visual landmark information gains control of the head direction signal at the lateral mammillary nuclei

• Published in: The Journal of neuroscience Vol. 35; no. 4; pp. 1354 - 1367
• Main Authors: Yoder, Ryan M, Peck, James R, Taube, Jeffrey S
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 28.01.2015
• Subjects: Action Potentials - drug effects; Action Potentials - physiology; Analysis of Variance; Animals; Cues; Excitatory Amino Acid Agonists - pharmacology; Female; Head; Head Movements; Mammillary Bodies - cytology; Mammillary Bodies - drug effects; Mammillary Bodies - physiology; N-Methylaspartate - pharmacology; Neural Pathways - drug effects; Neural Pathways - physiology; Neurons - drug effects; Orientation - drug effects; Orientation - physiology; Rats; Rats, Long-Evans; mammillary; visual; navigation; rat; landmark; spatial orientation
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.1418-14.2015

The neural representation of directional heading is conveyed by head direction (HD) cells located in an ascending circuit that includes projections from the lateral mammillary nuclei (LMN) to the anterodorsal thalamus (ADN) to the postsubiculum (PoS). The PoS provides return projections to LMN and ADN and is responsible for the landmark control of HD cells in ADN. However, the functional role of the PoS projection to LMN has not been tested. The present study recorded HD cells from LMN after bilateral PoS lesions to determine whether the PoS provides landmark control to LMN HD cells. After the lesion and implantation of electrodes, HD cell activity was recorded while rats navigated within a cylindrical arena containing a single visual landmark or while they navigated between familiar and novel arenas of a dual-chamber apparatus. PoS lesions disrupted the landmark control of HD cells and also disrupted the stability of the preferred firing direction of the cells in darkness. Furthermore, PoS lesions impaired the stable HD cell representation maintained by path integration mechanisms when the rat walked between familiar and novel arenas. These results suggest that visual information first gains control of the HD cell signal in the LMN, presumably via the direct PoS → LMN projection. This visual landmark information then controls HD cells throughout the HD cell circuit.