Visual Landmark Information Gains Control of the Head Direction Signal at the Lateral Mammillary Nuclei

Abstract

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.Key words: landmark; mammillary; navigation; rat; spatial orientation; visual IntroductionMost mammals are able to reliably perceive their momentary directional heading relative to the environment. In rodents, this directional perception is thought to be encoded by head direction (HD) cells, which are located throughout the limbic system (for review, see Taube, 2007). This HD cell signal appears to be generated from self-movement information that arrives from the vestibular system, but proprioceptive and/or motor efference cues also play a major role in updating the signal during movement (Taube and Burton, 1995; Blair et al., 1997; Stackman and Taube, 1997; Frohardt et al., 2006;Yoder et al., 2011a). Although these idiothetic cues are important for generating and updating the signal, visual landmarks dominantly control the preferred firing direction of the HD cell when these cues are available (Goodridge and Taube, 1995;Zugaro et al., 2003). The neural circuit responsible for providing this "landmark control" to the HD signal is not fully understood but is particularly important for our understanding of navigation and spatial learning.HD signal generation appears to occur within the reciprocal connections between the dorsal tegmental nuclei and the lateral mammillary nuclei (LMN), in which vestibular, motor efference copy, and optic flow information arrive from the medial vestibular nucleus, nucleus prepositus hypoglossi, supragenual nucleus, and paragigantocellular reticularis nucleus (Taube and Bassett, 2003;Song and Wang, 2005;Biazoli et al., 2006). From the LMN, the HD signal is projected bilaterally to the anterodorsal thalamus (ADN), which pr...

Decoding of neural data using cohomological learning

“…The GLM test found 90 moments of drift, lasting 2.01 seconds on average, that were dispersed throughout the experiment. Consistent with our findings, drift of the head direction representation has been previously reported in rodents [16,17,18,19]. Figure 4E shows that the discrepancy is mostly independent of the speed of the mouse, with a slight clockwise deviation at slow speeds and a slight counterclockwise deviation at higher speeds.…”

Laminar Localization and Projection-Specific Properties of Presubicular Neurons Targeting the Lateral Mammillary Nucleus, Thalamus, or Medial Entorhinal Cortex

“…The presubicular projection to the LMN relays visual information to the head direction system and may enhance head direction signal stability and accuracy (Yoder et al, 2015). The bursting nature of PrS → LMN-projecting neurons ensures that visual feedback is sent sparsely but efficiently with little delay to the subcortical generating circuit of the head direction signal.…”

Activity dependent feedback inhibition may maintain head direction signals in mouse presubiculum

“…Head direction signals transmitted via the thalamus are integrated in the presubiculum with visual information5 from visual9 and retrosplenial cortices7, and information from the hippocampal formation2. Presubicular head direction cells in layer 3 project to the entorhinal cortex1011 and may contribute to spatial firing of grid cells121314.…”