Backward inhibitory learning in honeybees: a behavioral analysis of reinforcement processing.

Hellstern, Frank; Malaka, Rainer; Hammer, Martin

doi:10.1101/lm.4.5.429

Cited by 76 publications

(80 citation statements)

References 43 publications

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“…This is in accordance with previous findings that backward-pairing of olfactory CS with gustatory US was not effective in achieving olfactory conditioning in insects and mammals (honeybees: Hellstern et al, 1997;crickets: Matsumoto and Mizunami, 2002;rats: Maier et al, 1976), although backward-pairing of visual CS with olfactory US was found to be effective for achieving conditioning in cockroaches (Lent and Kwon, 2004). …”

Section: Effects Of Conditioning On Odour Response Of Salivary Neuronessupporting

confidence: 81%

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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Section: Effects Of Conditioning On Odour Response Of Salivary Neuronessupporting

confidence: 81%

Classical conditioning of activities of salivary neurones in the cockroach

Watanabe

Mizunami

2006

Journal of Experimental Biology

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“…In order for classical conditioning to occur, the onset of the CS has to occur before the onset of the US. Simultaneous or reverse (backward) pairings yield very little to no learning (Hellstern et al, 1998). This result also contradicts the notion that simple pairings were sufficient for conditioning to occur.…”

Section: Invertebrate Classical Conditioningcontrasting

confidence: 49%

Cognition in Invertebrates

Menzel

Brembs

Giurfa

2007

Evolution of Nervous Systems

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“…Olfactory PER conditioning has become a versatile tool for the study of questions, not only in the field of comparative experimental psychology (e.g., Chandra and Smith 1998;Hellstern et al 1998;Deisig et al 2001Deisig et al , 2002Deisig et al , 2003, as originally planned by Takeda, but also in diversified fields such as olfactory perception (e.g., Vareschi 1971;Guerrieri et al 2005b;Reinhard et al 2010), neurobiology of olfaction and olfactory learning (e.g., Hammer 1993;Stopfer et al 1997;Faber et al 1999;Sandoz et al 2003;Rath et al 2011), molecular bases of memory (for review, see Menzel 1999;Schwärzel and Müller 2006), social bases of behavior in bees (e.g., Chaline et al 2005;Arenas and Farina 2008), and floral ecology (Wright et al 2002(Wright et al , 2005, to cite only a few examples. The basic premises of olfactory PER conditioning have also been adapted in other species, such as bumblebees (Laloi et al 1999;Riveros and Gronenberg 2009), stingless bees (McCabe et al 2007;Farina 2009, 2010), moths (Fan et al 1997;Fan and Hansson 2001;Daly et al 2004), and even ants, which do not have a proboscis but whose mouthpart movements can also be conditioned (Guerrieri and d'Ettorre 2010;Guerrieri et al 2011).…”

Section: Resultsmentioning

confidence: 99%

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Giurfa

Sandoz²

2012

Learn. Mem.

346

334

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The honeybee Apis mellifera has emerged as a robust and influential model for the study of classical conditioning, thanks to the existence of a powerful Pavlovian conditioning protocol, the olfactory conditioning of the proboscis extension response (PER). In 2011, the olfactory PER conditioning protocol celebrates 50 years since it was first introduced by Kimihisa Takeda in 1961. Here, we review its origins, developments, and perspectives in order to define future research avenues and necessary methodological and conceptual evolutions. We show that olfactory PER conditioning has become a versatile tool for the study of questions in extremely diverse fields in addition to the study of learning and memory and that it has allowed behavioral characterizations, not only of honeybees, but also of other insect species, for which the protocol was adapted. We celebrate, therefore, Takeda's original work and prompt colleagues to conceive and establish further robust behavioral tools for an accurate characterization of insect learning and memory at multiple levels of analysis.Classical conditioning (Pavlov 1927) is a form of conditioning in which a subject learns to associate a neutral stimulus (the "conditioned stimulus," or CS), which does not originally elicit a behavioral response, with a stimulus of biological significance (the "unconditioned stimulus," or US), which elicits an innate, often reflexive, response. Through this association, the originally neutral stimulus acquires the capacity to elicit a conditioned response.Decades of research on animal learning and memory have established some invertebrates (e.g., the sea hare, Aplysia californica, the fruit fly, Drosophila melanogaster, the honeybee, Apis mellifera) as standard models for the study of classical conditioning (Giurfa 2007b;Menzel et al. 2007). This success can be attributed to the fact that these animals can learn nonassociative as well as Pavlovian and operant associations and possess relatively simple nervous systems that allow retracing of these phenomena to the cellular and molecular levels in different kinds of laboratory preparations. Among these invertebrates, the honeybee, Apis mellifera, has emerged as a robust and influential model for the study of

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Backward inhibitory learning in honeybees: a behavioral analysis of reinforcement processing.

Cited by 76 publications

References 43 publications

Classical conditioning of activities of salivary neurones in the cockroach

Classical conditioning of activities of salivary neurones in the cockroach

Cognition in Invertebrates

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

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