Heterogeneous modulation of place cell firing by changes in context

Abstract

Hippocampal place cells show spatially localized activity that can be modulated by both geometric information (e.g., the distances and directions of features in the environment) and nongeometric information (e.g., colors, odors, and possibly behaviors). Nongeometric information may allow the discrimination of different spatial contexts. Understanding how nongeometric (or contextual) information affects hippocampal activity is important in light of proposals that the hippocampus may play a role in constructing a representation of spatial context. We investigated the contextual modulation of place cell activity by recording hippocampal place cells while rats foraged in compound contexts comprising black or white color paired with lemon or vanilla odor. Some cells responded to the color or odor changes alone, but most responded to varying combinations of both. Thus, we demonstrate, for the first time, that there is a heterogeneous input by contextual inputs into the hippocampus. We propose a model of contextual remapping of place cells in which the geometric inputs are selectively activated by subsets of contextual stimuli. Because it appears that different place cells are affected by different subsets of contextual stimuli, the representation of the entire context would require activity at the population level, supporting a role for the hippocampus in constructing a representation of spatial context.

Figure 1.

Pictorial representations of how contextual stimuli may modulate place cell activity. A, In the first possibility, all place cells are modulated by the same presynthesized context signal. B, In the second possibility, some place cells are modulated by different subsets of the contextual stimuli. Note that these pictures illustrate only how the context signal might be constructed, not how place cells remap after changes to these stimuli (a model of the latter is proposed in Fig. 4).

Figure 2.

The remapping patterns of seven place cells (A-G) across the contextual configurations (all complete data sets). A, A unit that had the same place field in all of the contexts (same condition r values: black lemon, 0.89; white lemon, 0.84; black vanilla, 0.91; white vanilla, 0.85; median different condition r values: black lemon and white lemon, 0.72; black lemon and black vanilla, 0.86; black lemon and white vanilla, 0.90; white lemon and black vanilla, 0.57; white lemon and white vanilla, 0.76; black vanilla and white vanilla 0.86). For this unit, all eight trials are displayed. For the units in B-G, only four trials are displayed, one for each context; these units had the same place fields in both trials of each context; the extra trials are omitted to save space. The letter to the left of each figure panel is a description of the context odor (L, lemon; V, vanilla) and refers to each map in that row. The context color is indicated by the dark and light boxes bordering each map (a dark box for the black contexts, a light box for the white contexts). The number inside each box in A indicates the peak firing rate for the corresponding map (in hertz); the two numbers inside each box in B-G indicate the peak firing rates for both trials in the corresponding context, with the rate for the displayed trial given first. Place fields are displayed as contour maps with five levels, each level representing a 20% portion of the peak firing rate for that map (color bar). B, A unit that fired only in the vanilla contexts (black and white), expressing the same place field in both vanilla contexts. C, A unit that fired only in the white contexts (lemon and vanilla). It had the same place field in both white contexts. D, A unit that fired only in the black lemon context. E, A unit that fired only in the lemon contexts (black and white) and remapped between them (compare with the unit in B). F, A unit that had the same place field in the black contexts (lemon and vanilla) but that showed a different place field in the white lemon context and did not fire in the white vanilla context (same condition r values: black lemon, 0.94; white lemon, 0.77; black vanilla, 0.80; median different condition r values: black lemon and white lemon, -0.05; black lemon and black vanilla, 0.74; white lemon and black vanilla, -0.08). G, A unit that fired in all contexts, with the same place field in the white contexts but two new fields in the black lemon and black vanilla contexts.

Figure 3.

Heterogeneous remapping of simultaneously recorded place cells. The remapping patterns of three sets of simultaneously recorded cells are shown (three cells in each set), with each set from a different rat (rats 1, 2, and 4). The remapping profile of each cell is illustrated with a four-map grouping, as used in Figure 2 (the same figure conventions are used here). Each row contains the simultaneously recorded cell set from one rat (the rat number is given to the left of the row). They are shown to illustrate that even simultaneously recorded cells demonstrated heterogeneous remapping profiles, and that these profiles were consistently observed in different rats. L, Lemon; V, vanilla.

Figure 4.

A model of the contextual remapping of place cells. In our model, the spatial inputs from the boundaries of the environment to a place cell, which are represented in the firing of what we call the boundary cell, are selectively activated by the contextual stimuli. In each panel, an example of a place cell from the present study is shown, with a figurative description of how the model can explain the remapping pattern that the unit shows. Heavy lines indicate strong connections, medium-weight lines indicate medium-strength connections, and dotted lines indicate connections that are not required to explain the remapping pattern of the unit. A, A unit that fires in both white contexts (lemon and vanilla) only. Its remapping pattern can be explained by its single boundary cell being activated by an elemental representation of white. B, To explain the complex remapping patterns observed here, some boundary cells would need to be activated by more than one contextual input so that the coactivity of both black and lemon contextual elements for this unit would be required to activate its boundary cell. C, Units that remap by showing different fields in different contexts (as opposed to units that remap by switching off in a particular context) require more than one boundary cell, activated by different contextual elements, to explain their remapping patterns. D, An alternative explanation of the remapping pattern for the cell shown in B. Subsets of contextual elements may be precombined before reaching the boundary cell level. Because we did not reliably see cells with identical fields in two nonoverlapping contexts only, we favor the explanation in B. L, Lemon; V, vanilla.