Pavlov's cockroach: classical conditioning of salivation in an insect.

Hidehiro Watanabe,Makoto Mizunami,Aldo Rustichini

doi:10.1371/journal.pone.0000529

Abstract

Secretion of saliva to aid swallowing and digestion is an important physiological function found in many vertebrates and invertebrates. Pavlov reported classical conditioning of salivation in dogs a century ago. Conditioning of salivation, however, has been so far reported only in dogs and humans, and its underlying neural mechanisms remain elusive because of the complexity of the mammalian brain. We previously reported that, in cockroaches Periplaneta americana, salivary neurons that control salivation exhibited increased responses to an odor after conditioning trials in which the odor was paired with sucrose solution. However, no direct evidence of conditioning of salivation was obtained. In this study, we investigated the effects of conditioning trials on the level of salivation. Untrained cockroaches exhibited salivary responses to sucrose solution applied to the mouth but not to peppermint or vanilla odor applied to an antenna. After differential conditioning trials in which an odor was paired with sucrose solution and another odor was presented without pairing with sucrose solution, sucrose-associated odor induced an increase in the level of salivation, but the odor presented alone did not. The conditioning effect lasted for one day after conditioning trials. This study demonstrates, for the first time, classical conditioning of salivation in species other than dogs and humans, thereby providing the first evidence of sophisticated neural control of autonomic function in insects. The results provide a useful model system for studying cellular basis of conditioning of salivation in the simpler nervous system of insects.

Highlights

Secretion of saliva to aid in the initial mastication, digestion and swallowing of food is an important physiological function found in many vertebrates and invertebrates
We investigated the effects of conditioning trials on salivary responses to odors, and we found that an odor paired with sucrose solution induced an increase in the level of salivation
We showed that (1) untrained cockroaches exhibited no salivation responses to vanilla or peppermint odor, (2) after differential conditioning trials in which an odor was paired with sucrose solution and another odor was presented alone, cockroaches exhibited salivation response to sucrose-associated odor but not to the odor presented alone, (3) the conditioning effect was maintained for 1 day after conditioning and (4) backward-pairing, conditioning stimulus (CS) alone and unconditioned stimulus (US) alone trials did not induce a conditioning effect

Summary

Introduction

Secretion of saliva to aid in the initial mastication, digestion and swallowing of food is an important physiological function found in many vertebrates and invertebrates. Pavlov [1] reported classical conditioning of salivation in dogs about a century ago, and this form of conditioning is the best-known example of classical conditioning. Many of basic principles of classical conditioning have been established by studying this important form of learning. As far as we know, conditioning of salivation has been reported only in dogs and humans [2,3]. Studies using operant and classical conditioning procedures showed that cockroaches have excellent learning capabilities [11,12,13,14,15]. Cockroaches exhibited excellent learning performance in an occasion setting paradigm in which visual context defines the contingency between olfactory CSs (conditioning stimuli) and gustatory USs (unconditioned stimuli) [16]

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Results

Conclusion