Bridging the gap between brain and behavior: cognitive and neural mechanisms of episodic memory

Abstract

The notion that non-human animals are capable of episodic memory is highly controversial. Here, we review recent behavioral work from our laboratory showing that the fundamental features of episodic memory can be observed in rats and that, as in humans, this capacity relies on the hippocampus. We also discuss electrophysiological evidence, from our laboratory and that of others, pointing to associative and sequential coding in hippocampal cells as potential neural mechanisms underlying episodic memory.

Figure 1. Receiver operating characteristics (ROCs) for recognition performance in humans and rats.

(a–c) Performance of humans in verbal recognition memory. (d–f) Performance of rats on odor recognition memory. (d) Normal rats tested at a 30-min memory delay. Insets show recollection estimates (R), which correspond to the mean Y intercept obtained from the ROC of individual subjects, and familiarity estimates (F) which correspond to the mean degree of curvature (d′) of individual ROCs (transformed into a probability in order to facilitate comparisons with R). (e) Control rats and rats with selective hippocampal lesions at 30-min delay; also shown is the ROC curve for Controls with the estimated recollection component (cf. Figure 1c) algebraically removed (Con-F). (f) Control rats tested at a 75-min memory delay. C, control animals; H, animals with lesions to the hippocampus; *, p < .05.

Figure 2. Odor recognition task for ROC analyses in rats.

In each session, rats initially dug for a 1/4 Cheerio reward in each of 10 cups. Each cup was filled with playground sand scented with a distinct odor and presented individually in the front of the home cage. For each of the subsequent 20 test odors, the animal could obtain an additional reward by digging in the test cup if the odor was new (i.e., non-match) or by refraining from digging in the test cup and approaching an alternate empty cup at the back of the cage if the odor was old (i.e., match). We recorded correct responses (hits) and incorrect responses (false alarms) at the alternate cup.

Figure 3. Sequential order and recognition tasks.

(a) Left: presentation of sample sequence. Letters A–E designate the five randomly selected odors presented in a particular series. Right: examples of the sequential order and recognition probe for that series. +  =  reinforced odor; −  =  nonreinforced odor. (b) Performance on the sequential order probe types, grouped according to the lag (number of intervening elements) between items in the probe test. (c) Performance on the recognition probes. X designates a randomly selected odor that was not presented in the series and used as the alternative choice. Hippocampus refers to animals with hippocampal damage. *, p < .05.

Figure 4. Odor guided, continuous non-matching-to-sample task.

Trial n represents a non-match trial where the odor differs from that presented on the previous trial, and the rat digs to find a buried reward. On the next trial (n + 1), the same scent is repeated, but in a different location. As no reward was available, animals quickly learned not to dig on these match trials and to turn away from the cup. On the subsequent trial (n + 2), the odor again differs from that of the previous trial, and the animal digs for a buried reward. Note that the position of the cup is independent of the match/non-match contingency.

Figure 5. Hippocampal neuronal activity as rats perform a delayed alternation task.

(a) Schematic view of the modified T maze. Rats performed a continuous alternation task in which they traversed the central stem of the apparatus on each trial and then alternated between left and right turns at the T junction. Reinforcement for correct alternations was provided at water ports (small circles) on the end of each choice arm. The rat returned to the base of the stem via connecting arms, and then traversed the central stem again on the next trial. For analysis of neural firing patterns, left-turn (blue arrow) and right-turn (red arrow) trials were distinguished. Only trials that involved correct responses were included in the analyses. (b) Schematic of the stem of the T maze indicating divisions of the central portion of the stem into the four sectors used in the data analyses. (c) Examples of hippocampal cells that are active when the rat is traversing the central stem. These cells fire almost exclusively during either left-turn or right-turn trials. In each example, the paths taken by the animals on the central stem are plotted in the left panel (blue: left-turn trial; red: right-turn trial). In the middle panels, the location of the rat when individual spikes occurred is indicated separately for left-turn trials (blue dots on light grey path), and right-turn trials (red dots on dark grey path). In the right panel, the mean firing rate of the cell for each sector, adjusted for variations in firing associated with covariates (see text), is shown separately for left-turn trials (blue) and right-turn trials (red).