Way-finding in displaced clock-shifted bees proves bees use a cognitive map

Significance The question of the computational capacities of the brains of widely separated genera of animals is of interest to behavioral biologists, comparative psychologists, computational neuroscientists, philosophers of mind, and—we believe—much of the scientific community. Half a century ago, the claim that any nonhuman animal had a cognitive map was deeply controversial. If true, it greatly favored a computational theory of mind, as opposed to an antirepresentational behaviorist theory. Now that it is well established by behavioral and neurobiological evidence that rodents have a metric cognitive map, the question of whether insects do is a frontier question, the answer to which has broad implications in several disciplines. Mammals navigate by means of a metric cognitive map. Insects, most notably bees and ants, are also impressive navigators. The question whether they, too, have a metric cognitive map is important to cognitive science and neuroscience. Experimentally captured and displaced bees often depart from the release site in the compass direction they were bent on before their capture, even though this no longer heads them toward their goal. When they discover their error, however, the bees set off more or less directly toward their goal. This ability to orient toward a goal from an arbitrary point in the familiar environment is evidence that they have an integrated metric map of the experienced environment. We report a test of an alternative hypothesis, which is that all the bees have in memory is a collection of snapshots that enable them to recognize different landmarks and, associated with each such snapshot, a sun-compass–referenced home vector derived from dead reckoning done before and after previous visits to the landmark. We show that a large shift in the sun-compass rapidly induced by general anesthesia does not alter the accuracy or speed of the homeward-oriented flight made after the bees discover the error in their initial postrelease flight. This result rules out the sun-referenced home-vector hypothesis, further strengthening the now extensive evidence for a metric cognitive map in bees.