The Memories of Butterflies

In a study published yesterday in Public Library of Science ONE, Georgetown University biologists gave mild shocks to tobacco hornworm caterpillars while exposing the caterpillars to particular odors.

After the hornworms built coccoons and emerged as moths -- a process that involves the reorganization of both brain and nervous system -- they still avoided the smells that once brought them shocks.

The findings "challenge a broadly-held popular view of lepidopteran metamorphosis: that the caterpillar is essentially broken down entirely, and its  omponents reorganized into a butterfly or moth," wrote the researchers.

Led by evolutionary ecologist Martha Weiss, they suspected that larval memories, if maintained at all, would be stored in the so-called mushroom bodies -- areas of the brain that receive information directly from the antennae.

Since mushroom body neurons that accumulate early in larval development are lost during metamorphosis, the hypothesis was easy to test: the researchers conditioned the caterpillars at different ages.

As they predicted, caterpillars that learned late to associate shock and odor kept the memory into adulthood. Those who made the association early emerged from their coccoons without remembering.

Insects that undergo complete metamorphosis experience enormous changes in both morphology and lifestyle. The current study examines whether larval experience can persist through pupation into adulthood in Lepidoptera, and assesses two possible mechanisms that could underlie such behavior: exposure of emerging adults to chemicals from the larval environment, or associative learning transferred to adulthood via maintenance of intact synaptic connections. Fifth instar Manduca sexta caterpillars received an electrical shock associatively paired with a specific odor in order to create a conditioned odor aversion, and were assayed for learning in a Y choice apparatus as larvae and again as adult moths. We show that larvae learned to avoid the training odor, and that this aversion was still present in the adults.