Dynamics of Mismatch Correction in the Hippocampal Ensemble Code for Space: Interaction between Path Integration and Environmental Cues

Abstract

Populations of hippocampal neurons were recorded simultaneously in rats shuttling on a track between a fixed reward site at one end and a movable reward site, mounted in a sliding box, at the opposite end. While the rat ran toward the fixed site, the box was moved. The rat returned to the box in its new position. On the initial part of all journeys, cells fired at fixed distances from the origin, whereas on the final part, cells fired at fixed distances from the destination. Thus, on outward journeys from the box, with the box behind the rat, the position representation must have been updated by path integration. Farther along the journey, the place field map became aligned on the basis of external stimuli. The spatial representation was quantified in terms of population vectors. During shortened journeys, the vector shifted from an alignment with the origin to an alignment with the destination. The dynamics depended on the degree of mismatch with respect to the full-length journey. For small mismatches, the vector moved smoothly through intervening coordinates until the mismatch was corrected. For large mismatches, it jumped abruptly to the new coordinate. Thus, when mismatches occur, path integration and external cues interact competitively to control place-cell firing.When the same box was used in a different environment, it controlled the alignment of a different set of place cells. These data suggest that although map alignment can be controlled by landmarks, hippocampal neurons do not explicitly represent objects or events.

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

“…Firing fields were otherwise unaltered by such rigid rotations. This nearly ideal control of firing fields by specific stimuli is also in agreement with previous work (O'Keefe and Conway 1978; Muller and Kubie 1987; Sharp et al 1990; Gothard et al 1996; Cressant et al 1997). (c) The only effect of removing one card and rotating the other was to cause uniform rotations of all firing fields.…”

“…Additional studies by Sharp et al 1990 and Skaggs and McNaughton 1998 indicate that some place cells may have similar fields in two visually similar parts of an apparatus (in line with the combinatorial view), but that other cells may reliably fire in only one of the two regions, perhaps based on the use of position tracking by self-motion information (consistent with a spatial representation). Similar conclusions can be drawn from the study of Gothard et al 1996.…”

Is there a geometric module for spatial orientation? Insights from a rodent navigation model.

“…On the neural level, these data have been related to the properties of place cells in the areas CA3-CA1 of the hippocampus, since their firing fields develop during unrewarded exploration (Hill, 1978;Wilson & McNaughton, 1993), persist in darkness (Quirk, Muller, & Kubie, 1990), and depend on multiple sensory stimuli (Gothard et al, 1996;O'Keefe & Burgess, 1996).…”

The hippocampal debate: are we asking the right questions?

“…Interestingly, spatial cues are sometimes represented discretely: on a linear track, cells differentiate the two directions of travel [67,101,109,174]. However, when allowed to experience all directions without limitations (such as when foraging within an open environment), cells do not show any directional dependence at all [101,128,130].…”

“…On other alternation tasks (such as back-and-forth along a linear track, i.e. alternating directions), cells differentiate the two directions [67,101,109,174].…”