The hippocampus and memory for "what," "where," and "when"

Abstract

Previous studies have indicated that nonhuman animals might have a capacity for episodic-like recall reflected in memory for "what" events that happened "where" and "when". These studies did not identify the brain structures that are critical to this capacity. Here we trained rats to remember single training episodes, each composed of a series of odors presented in different places on an open field. Additional assessments examined the individual contributions of odor and spatial cues to judgments about the order of events. The results indicated that normal rats used a combination of spatial ("where") and olfactory ("what") cues to distinguish "when" events occurred. Rats with lesions of the hippocampus failed in using combinations of spatial and olfactory cues, even as evidence from probe tests and initial sampling behavior indicated spared capacities for perception of spatial and odor cues, as well as some form of memory for those individual cues. These findings indicate that rats integrate "what," "where," and "when" information in memory for single experiences, and that the hippocampus is critical to this capacity.

Figure 1

An example (B vs. C) trial for a standard test and odor and spatial probes. In the sample phase of every trial, the rat is presented with four odors in series (A+ → B+ → C+ → D+), each at a different location on a platform. In the following test phase, odors B and C are presented in their sample locations in the standard choice test, or next to each other in the odor probe, or two nonodorous stimuli are presented in the sample locations of B and C in the spatial probe. “+,” reinforced stimulus; arrow on the platform, position of the rat at the starting point (arrowhead corresponds to the rat's head); star symbol, the experimenter's fixed position throughout testing.

Figure 2

Performance (mean ± SE) of normal rats (n=14). (A) Comparison of performance versus percentage of correct first approaches on standard choice tests. (B) Performance on probe tests and accompanying standard choice tests. Dashed line: chance performance (50%).

Figure 3

Detection of odors on the platform by normal rats (n=4). (A) First approach (○) and choice (♦) responses (mean ± SE). Dashed line: chance. (B) Proximity to cups in the first approach (mean ± SE). 0 cm, rat's nose is over the cup; 3 cm, rat's nose is within 3 cm; 6 cm, rat's nose is within 6 cm.

Figure 4

Reconstructions of the smallest and largest brain lesions for sham-control and H groups. Lesions were reconstructed on coronal sections adapted from Swanson (1992) at AP -3.90 mm, -5.25 mm, and -6.06 mm. The largest lesions are indicated with light gray, smallest lesions with dark gray.

Figure 5

Postsurgery performance (mean ± SE) of sham-control and H groups. (A) Comparison of performance vs. percentage of correct first approaches on standard choice tests. (B) Performance on probe tests and accompanying standard choice tests. Dashed line: chance.