Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes

Abstract

Successful navigation requires a constantly updated neural representation of directional heading, which is conveyed by head direction (HD) cells. The HD signal is predominantly controlled by visual landmarks, but when familiar landmarks are unavailable, self-motion cues are able to control the HD signal via path integration. Previous studies of the relationship between HD cell activity and path integration have been limited to two or more arenas located in the same room, a drawback for interpretation because the same visual cues may have been perceptible across arenas. To address this issue, we tested the relationship between HD cell activity and path integration by recording HD cells while rats navigated within a 14-unit T-maze and in a multiroom maze that consisted of unique arenas that were located in different rooms but connected by a passageway. In the 14-unit T-maze, the HD signal remained relatively stable between the start and goal boxes, with the preferred firing directions usually shifting <45° during maze traversal. In the multiroom maze in light, the preferred firing directions also remained relatively constant between rooms, but with greater variability than in the 14-unit maze. In darkness, HD cell preferred firing directions showed marginally more variability between rooms than in the lighted condition. Overall, the results indicate that self-motion cues are capable of maintaining the HD cell signal in the absence of familiar visual cues, although there are limits to its accuracy. In addition, visual information, even when unfamiliar, can increase the precision of directional perception.

Decoding signal processing in thalamo-hippocampal circuitry: implications for theories of memory and spatial processing

“…Hippocampal place cells are also closely coupled to head-direction cells, and hippocampal spatial representation is functionally related to the directional system (Knierim et al, 1995;Knierim et al, 1998). From external sensory signals, visual (landmark) information is the most potent source maintaining and updating activity of head-direction cells (Yoder et al, 2011a). The current hypothesis of how visual landmark cues control directional tuning suggests that the postsubiculum (Goodridge and Taube, 1997) and the retrosplenial cortex (Clark et al, 2010) might transfer visual landmark information to spatial signals within the limbic system (Yoder et al, 2011b).…”

Do the anterior and lateral thalamic nuclei make distinct contributions to spatial representation and memory?

“…Control by landmarks appears to be predominantly guided by cues located in the distal background of the environment (Yoganarasimha et al, 2006;Zugaro et al, 2001). Further, the preferred direction of anterodorsal thalamic cells can be maintained in the absence of visual information and when entering novel environments, suggesting that self-movement cues (e.g., vestibular, motor, and proprioceptive stimuli) contribute to the stability of directional tuning (Goodridge et al, 1998;Yoder et al, 2011b). Thus, the anterodorsal thalamus has a pivotal position between self-motion and visual systems to provide a coherent percept of spatial orientation in an environment in relation to distal landmarks.…”

“…The anterior thalamus receives projections from the mammillary nuclei, which process visual-spatial and self-movement information (Taube, 2007;Yoder et al, 2011b).…”

Collective strategy for obstacle navigation during cooperative transport by ants

“…This type of behavior is akin to problem solving, and has been studied primarily in individuals rather than groups. For example, maze-solving has been studied in many taxa including rats (Mulder et al, 2004;Yoder et al, 2011) and single-celled slime molds (Nakagaki et al, 2000;Reid and Beekman, 2013;Reid et al, 2012). Groups making serial decisions face the additional challenge of maintaining consensus -defined as agreeing on a single option (Sumpter and Pratt, 2009).…”