Classical Olfactory Conditioning in the Cockroach Periplaneta americana

Watanabe, Hidehiro; Kobayashi, Yuko; Sakura, Midori; Matsumoto, Y.; Mizunami, Makoto

doi:10.2108/zsj.20.1447

Cited by 63 publications

(71 citation statements)

References 54 publications

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“…This was because cockroaches exhibit preferences for sucrose solution or an odor associated with it and avoidance of sodium chloride solution or an odor associated with it (Sakura & Mizunami, 2001;Watanabe, Kobayashi, Sakura, Matsumoto, & Mizunami, 2003), but they exhibit an increase of the level of salivation in response to sucrose solution or sodium chloride solution or to an odor associated with either of them (Watanabe & Mizunami, 2006). This is analogous to that dogs exhibit salivation in response to food or acid solution or a sensory stimulus associated with either of them (Pavlov, 1927).…”

Section: Discussionmentioning

confidence: 99%

Context-dependent olfactory learning monitored by activities of salivary neurons in cockroaches

Matsumoto¹,

Matsumoto²,

Watanabe³

et al. 2012

Neurobiology of Learning and Memory

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Context-dependent discrimination learning, a sophisticated form of nonelemental associative learning, has been found in many animals, including insects. The major purpose of this research is to establish a method for monitoring this form of nonelemental learning in rigidly restrained insects for investigation of underlying neural mechanisms. We report context-dependent olfactory learning (occasion-setting problem solving) of salivation, which can be monitored as activity changes of salivary neurons in immobilized cockroaches, Periplaneta americana. A group of cockroaches was trained to associate peppermint odor (conditioned stimulus, CS) with sucrose solution reward (unconditioned stimulus, US) while vanilla odor was presented alone without pairing with the US under a flickering light condition (1.0 Hz) and also trained to associate vanilla odor with sucrose reward while peppermint odor was presented alone under a steady light condition. After training, the responses of salivary neurons to the rewarded peppermint odor were significantly greater than those to the unrewarded vanilla odor under steady illumination and those to the rewarded vanilla odor was significantly greater than those to the unrewarded peppermint odor in the presence of flickering light.Similar context-dependent responses were observed in another group of cockroaches trained with the opposite stimulus arrangement. This study demonstrates context-dependent olfactory learning of salivation for the first time in any vertebrate and invertebrate species, which can be monitored by activity changes of salivary neurons in restrained cockroaches.

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Section: Discussionmentioning

confidence: 99%

Context-dependent olfactory learning monitored by activities of salivary neurons in cockroaches

Matsumoto¹,

Matsumoto²,

Watanabe³

et al. 2012

Neurobiology of Learning and Memory

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“…We have shown that cockroaches have excellent olfactory learning capabilities (Sakura & Mizunami, 2001;Sakura, Okada, & Mizunami, 2002;Watanabe, Kobayashi, Sakura, Matsumoto & Mizunami, 2003) and that cockroaches exhibit conditioning of salivation, i.e., they exhibit increased levels of salivation in response to an odor applied to an antenna after the odor (CS) is paired with sucrose solution (US) applied to the mouth or an antenna (Watanabe & Mizunami, 2006;Watanabe, Sato, Kuramochi, Nishino, & Mizunami, 2008). This conditioning can be monitored by changes in activities of salivary neurons in immobilized animals (Watanabe & Mizunami, 2006;Watanabe et al, 2008), thus allowing for studying the effects of local microinjections of drugs into specific brain areas on conditioning.…”

Section: Introductionmentioning

confidence: 90%

Critical roles of mecamylamine-sensitive mushroom body neurons in insect olfactory learning

Watanabe

Matsumoto

Nishino

et al. 2011

Neurobiology of Learning and Memory

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“…The classical conditioning procedures used in this study were modified from those used for cockroaches (Watanabe et al, 2003) and crickets (Matsumoto and Mizunami, 2002;Matsumoto and Mizunami, 2004). Five sets of forward or backward CS/US pairing trials were performed on immobilized animals during recording of the activities of the SDN.…”

Section: Classical Conditioning Proceduresmentioning

confidence: 99%

“…Cockroaches can be trained to associate olfactory CSs with gustatory USs by an operant (Sakura and Mizunami, 2001;Sakura et al, 2002) or a classical conditioning procedure (Watanabe et al, 2003). The latter procedure is effective for both freely moving and restrained cockroaches.…”

Section: Introductionmentioning

confidence: 99%

Classical conditioning of activities of salivary neurones in the cockroach

Watanabe

Mizunami

2006

Journal of Experimental Biology

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SUMMARY Secretion of saliva to aid swallowing and digestion is a basic physiological function found in many vertebrates and invertebrates. For mammals, classical conditioning of salivation in dogs was reported by Pavlov a century ago. However, conditioning of salivation or of related neural activities in non-mammalian species has not been reported. In many species of insects, salivation is regulated by salivary neurones. In this study, we found that salivary neurones of the cockroach Periplaneta americanaexhibited a strong response to sucrose solution applied to the mouth and a weak response to odours applied to an antenna, and we studied the effect of conditioning on the activities of salivary neurones. After three sets of differential conditioning trials in which an odour was presented just before the presentation of sucrose solution and the other odour was presented alone,the response of salivary neurones to sucrose-associated odour significantly increased but that to the odour presented alone was unchanged. Backward pairing trials in which an odour was presented after the presentation of sucrose solution were not effective in achieving conditioning. Our study of the change in the level of saliva secretion in response to electrical stimulation of salivary neurones suggested that the magnitude of increase in odour response of salivary neurones by conditioning is sufficient to lead to an increased level of salivation. This study suggests classical conditioning of salivation in an insect.

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Classical Olfactory Conditioning in the Cockroach Periplaneta americana

Cited by 63 publications

References 54 publications

Context-dependent olfactory learning monitored by activities of salivary neurons in cockroaches

Context-dependent olfactory learning monitored by activities of salivary neurons in cockroaches

Critical roles of mecamylamine-sensitive mushroom body neurons in insect olfactory learning

Classical conditioning of activities of salivary neurones in the cockroach

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