Framing Spatial Cognition: Neural Representations of Proximal and Distal Frames of Reference and Their Roles in Navigation

Abstract

The most common behavioral test of hippocampus-dependent, spatial learning and memory is the Morris water task, and the most commonly studied behavioral correlate of hippocampal neurons is the spatial specificity of place cells. Despite decades of intensive research, it is not completely understood how animals solve the water task and how place cells generate their spatially specific firing fields. Based on early work, it has become the accepted wisdom in the general neuroscience community that distal spatial cues are the primary sources of information used by animals to solve the water task (and similar spatial tasks) and by place cells to generate their spatial specificity. More recent research, along with earlier studies that were overshadowed by the emphasis on distal cues, put this common view into question by demonstrating primary influences of local cues and local boundaries on spatial behavior and place-cell firing. This paper first reviews the historical underpinnings of the “standard” view from a behavioral perspective, and then reviews newer results demonstrating that an animal's behavior in such spatial tasks is more strongly controlled by a local-apparatus frame of reference than by distal landmarks. The paper then reviews similar findings from the literature on the neurophysiological correlates of place cells and other spatially-correlated cells from related brain areas. A model is proposed by which distal cues primarily set the orientation of the animal's internal spatial coordinate system, via the head direction cell system, whereas local cues and apparatus boundaries primarily set the translation and scale of that coordinate system.

Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local–global reference frames

“…B 369: 20130369 with the boundaries of the environment (i.e. they may set the translational phase of the grid) [33,34,72]. Head direction cells are thought to set the orientation of the grid; these cells themselves are known to be reset by prominent visual landmarks when they become misaligned with the allocentric reference frame defined by external landmarks [73].…”

Sex differences after environmental enrichment and physical exercise in rats when solving a navigation task

“…Environmentally enriched animals perform better on cognitive tests conducted when they are adults, with spatial tasks being frequently employed for this purpose (Harris, D'Eath, & Healy, 2009;Kolb & Gibb, 1991;Leggio et al, 2005;Nilsson, Perfilieva, Johansson, Orwar, & Eriksson, 1999;Pham, Söderström, Winbald, & Mohammed, 1999). Among spatial tasks, the Morris water navigation task (Morris, 1981) is probably the procedure most widely used to study spatial learning, with the hippocampus identified as a crucial brain area for spatial learning (for reviews, see Knierim & Hamilton, 2010;Pearce, 2009;Sutherland & Hamilton, 2004). Similar to EE, enhanced performance, in both humans and animals, is found with physical exercise, like voluntary wheel running in rats (for a review, see Sherwin, 1998).…”

Environmental stability modulates the role of path integration in human navigation

“…These results imply a common solution for the interaction of path integration and landmarks in human and animal navigation (Zhao & Warren, 2015). Specifically, visual landmarks reset the path integrator by reorienting the head direction cell system, the grid cell system, and the directional coordinates of the place cell system (Knierim & Hamilton, 2011;Valerio & Taube, 2012;Yoder et al, 2011).…”

“…Because path integration drifts and error accumulates rapidly (e.g., Loomis et al, 1993), a navigator can take an environmental 'fix' on visual landmarks and re-initialize the path integrator, thereby facilitating reorientation and selflocalization (Etienne & Jeffery, 2004;Etienne, Maurer, Boulens, Levy, & Rowe, 2004;Valerio & Taube, 2012; see also Knierim & Hamilton, 2011). Covertly shifting a visual beacon not only captures an animal's homing behavior, but also induces a corresponding shift in the spatial tuning of underlying neural mechanisms (e.g., place cells, head direction cells, and grid cells; Hafting et al, 2005;Knierim, Kudrimoti, & McNaughton, 1998;Taube et al, 1990).…”