The Neurobiology of Mammalian Navigation

Abstract

Mammals have evolved specialized brain systems to support efficient navigation within diverse habitats and over varied distances, but while navigational strategies and sensory mechanisms vary across species, core spatial components appear to be widely shared. This review presents common elements found in mammalian spatial mapping systems, focusing on the cells in the hippocampal formation representing orientational and locational spatial information, and 'core' mammalian hippocampal circuitry. Mammalian spatial mapping systems make use of both allothetic cues (space-defining cues in the external environment) and idiothetic cues (cues derived from self-motion). As examples of each cue type, we discuss: environmental boundaries, which control both orientational and locational neuronal activity and behaviour; and 'path integration', a process that allows the estimation of linear translation from velocity signals, thought to depend upon grid cells in the entorhinal cortex. Building cognitive maps entails sampling environments: we consider how the mapping system controls exploration to acquire spatial information, and how exploratory strategies may integrate idiothetic with allothetic information. We discuss how 'replay' may act to consolidate spatial maps, and simulate trajectories to aid navigational planning. Finally, we discuss grid cell models of vector navigation.

Neurobiological successor features for spatial navigation

“…The introduction of internal barriers into an environment provides a succinct test for geometric theories of spatial firing and has been studied in both experimental and theoretical settings. Indeed, the predictable allocentric responses of biological BVCs to inserted barriers provides some of the most compelling evidence for their existence (Lever et al, 2009;Poulter, Hartley, & Lever, 2018). In CA1 place cells, barrier insertion promotes an almost immediate duplication of place fields ) which may then be then lost or stabilised during subsequent exploration (Barry et al, 2006;Barry & Burgess, 2007).…”

Neural activity in a hippocampus-like region of the teleost pallium are associated with navigation and active sensing

“…Lastly, and most interestingly, discharge of these DDi units near landmarks is associated with active sensing, i.e., increased EODr and sampling density and scanning behavior (B-scans). Rodents use head-scans as 'a spatially directed investigative behavior' (Poulter et al 2018); there is a clear functional analogy between head-scans and B-scans. An important recent study showed that headscans drive formation or strengthening of place field discharge of hippocampal cells (Monaco et al 2014).…”

Cognitive swarming in complex environments with attractor dynamics and oscillatory computing

“…Spatial cognition in rodents has been extensively studied in non-naturalistic environments such as linear or circular tracks, radial arm mazes, and T-mazes, or small open-field arenas such as squares or cylinders of approximately 1-2 m 2 area. Such experimental conditions have allowed individual place fields of hippocampal pyramidal neurons (O'Keefe and Dostrovsky, 1971) and the activity of other spatial cells (Knierim, 2006;Moser et al, 2008;Savelli et al, 2008;Poulter et al, 2018;Wang et al, 2018) to be exquisitely controlled and analyzed, leading to a detailed neural coding account of distributed representations that subserve spatial learning, memory, and planning in mammals (O'Keefe and Nadel, 1978;Moser and Paulsen, 2001;Knierim and Hamilton, 2011;Monaco and Abbott, 2011;Pfeiffer and Foster, 2013;Hartley et al, 2014;Burgess, 2014;Schiller et al, 2015;Foster, 2017), potentially extending to general cognitive computations in humans (Bellmund et al, 2018;Kunz et al, 2019). However, the multiplicity of Poisson-distributed hippocampal place fields exposed in larger environments (Fenton et al, 2008;Rich et al, 2014) and species differences in mapping 3-dimensional contexts (Yartsev and Ulanovsky, 2013;Casali et al, 2019) suggest large and/or complex environments as the next frontier in understanding spatial navigation.…”