Memory influences on hippocampal and striatal neural codes: effects of a shift between task rules

Abstract

Interactions with neocortical memory systems may facilitate flexible information processing by hippocampus. We sought direct evidence for such memory influences by recording hippocampal neural responses to a change in cognitive strategy. Well-trained rats switched (within a single recording session) between the use of place and response strategies to solve a plus maze task. Maze and extramaze environments were constant throughout testing. Place fields demonstrated (in-field) firing rate and location-based reorganization [Leutgeb, S., Leutgeb, J. K., Barnes, C. A., Moser, E. I., McNaughton, B. L., & Moser, M. B. (2005). Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science, 309, 619-623] after a task switch, suggesting that hippocampus encoded each phase of testing as a different context, or episode. The task switch also resulted in qualitative and quantitative changes to discharge that were correlated with an animal's velocity or acceleration of movement. Thus, the effects of a strategy switch extended beyond the spatial domain, and the movement correlates were not passive reflections of the current behavioral state. To determine whether hippocampal neural responses were unique, striatal place and movement-correlated neurons were simultaneously recorded with hippocampal neurons. Striatal place and movement cells exhibited a response profile that was similar, but not identical, to that observed for hippocampus after a strategy switch. Thus, retrieval of a different memory led both neural systems to represent a different context. However, hippocampus may play a special (though not exclusive) role in flexible spatial processing since correlated firing amongst cell pairs was highest when rats successfully switched between two spatial tasks. Correlated firing by striatal cell pairs increased following any strategy switch, supporting the view that striatum codes change in reinforcement contingencies.

Figure 1

Schematic illustrations of the three behavioral test conditions. Bars across the top of each column show the sequence of events. For each condition, top-down views of the plus maze contain arrows indicating the correct path taken by rats. The 1-min period of darkness was meant to facilitate retrieval of the memory appropriate for Phase 2.

Figure 2

A) Rats were first trained to perform 10 trials on a plus maze according to either a place or response strategy. Choice accuracy rapidly improved for place-trained rats (filled circles). Although rats eventually learned to perform according to a response strategy (open circles), the learning was much slower. B-D) Choice accuracy during Phase 1 (filled circles) remained high during both place and response training. Phase 2 performance (open circles) also remained high across test days for the Between-Strategy and the Within-Strategy conditions.

Figure 3

The distribution of difference indices (DI) for field reliability, within-field firing rate specificity and location specificity for HPC and STR neurons. DIs quantify the magnitude of change after a strategy switch. The behavioral conditions are denoted as follows: open bars-Between-Strategy (B-S) conditions, hatched bars-Within-Strategy: Place-Place (P-P) condition. It can bee seen that many (but not all) neurons responded to the cognitive shift while other neurons did not. Also note that neural responses were bidirectional in that increased and decreased values were observed for different cells.

Figure 4

Individual color density figures show changes in location specific firing by HPC place cells after a strategy switch. A-left half: The leftmost plot shows that during Phase 1, very little firing was observed. The rightmost plot shows that a place field appeared on the south maze arm, but that this field was “conditional” in that it was observed only when the rat arrived on the south arm from the east, but not west, arm (shown immediately below). Spatial correlation scores are indicated between the summary plots for each Phase of test. ‘%correct’ refers to the percent of trials in which a correct response was observed per phase. A-right half: Place field responses of two simultaneously recorded place cells during Phases 1 and 2 (leftmost and rightmost) of test. The first cell (top row) showed redistributed firing patterns after the task rule switched, while the second cell (bottom row) showed a persistent place field on the west arm. B: Two examples of the dramatic effects of cognitive shift on place field locations during the Within-Strategy: Place-Place condition. [Calibration bar applies to all examples]

Figure 5

Individual illustrations of STR place cell responses to the different switches in task rule. Often dramatic reorganization was observed for after all test conditions. Note that similar ‘conditional’ firing was observed for STR place fields (A, left half). The place field for the top left cell recorded in the Between-Strategy condition was observed primarily when the rat entered the south arm from the east, but not west, start location.

Figure 6

Summary of the correlation analysis for pairs of cells recorded in hippocampus or striatum. The absolute (abs) value of the correlation coefficients show that HPC pairs increased correlative discharge only during the Within-Strategy condition, suggesting that output signal strength may be stronger when flexible spatial processing is required. In contrast, STR correlative discharge increased after both Between-Strategy and Within-Strategy conditions.

Figure 7

Individual cell examples of changes in acceleration correlated firing by HPC neurons. Three examples are provided per test condition. For each example, the firing rate per unit of acceleration is shown for Phase 1 trials (open circles) and Phase 2 trials (closed circles). It can be seen that some cells developed or lost the behavioral correlate, or did not change. (r and a-values are shown for Phase 1 (r₁, a₁) and Phase 2 (r₂, a₂).

Figure 8

Individual cell examples of changes in acceleration correlated firing by STR neurons. As in Fig. 7, a variety of responses were observed.