What, where and when: deconstructing memory

Abstract

The ability of animals to remember the what, where and when of a unique past event is used as an animal equivalent to human episodic memory. We currently view episodic memory as reconstructive, with an event being remembered in the context in which it took place. Importantly, this means that the components of a what, where, when memory task should be dissociable (e.g. what would be remembered to a different degree than when). We tested this hypothesis by training hummingbirds to a memory task, where the location of a reward was specified according to colour (what), location (where), and order and time of day (when). Although hummingbirds remembered these three pieces of information together more often than expected, there was a hierarchy as to how they were remembered. When seemed to be the hardest to remember, while errors relating to what were more easily corrected. Furthermore, when appears to have been encoded as a combination of time of day and sequence information. As hummingbirds solved this task using reconstruction of different memory components (what, where and when), we suggest that similar deconstructive approaches may offer a useful way to compare episodic and episodic-like memories.

Keywords: cognition; episodic-like memory; hummingbird; memory reconstruction; what–where–when.

Figure 1.

Schematic showing the two arrays of Experiment 1 and also the flower categorizations (e.g. correct or a what error) for morning trials.

Figure 2.

Proportion of first choices of each type in Experiment 1. The solid line at 0.125 represents chance for when, where and correct choices. The dashed line at 0.375 represents chance for what choices. The dotted line at 0.25 represents chance for all-wrong choices. Birds made correct choices significantly more often than chance, fewer all-wrong errors than chance, fewer what errors than chance and more when errors than chance.

Figure 3.

Hummingbird choices were corrected non-randomly. 47/134 choices of the birds’ first decision were correct, while 87/134 were errors. Where birds made what errors (whether on their first, second or third choice), 86% of the next choices were to the correct flower. However, if birds made a where, when or all-wrong error, 75% of the next choices were also wrong.

Figure 4.

The number of birds that made their first choice to the morning and afternoon flowers at the early, midday and late tests. Striped portions of bars represent choices of the afternoon rewarded flower, clear bars represent choices of the morning rewarded flower and dotted bars represent choices of unrewarded flowers.