Octopamine‐like immunoreactivity in the brain and subesophageal ganglion of the honeybee

Kreissl, Sabine; Eichmüller, Stefan B.; Bicker, Gerd; Rapus, Jürgen; Eckert, Manfred

doi:10.1002/cne.903480408

Cited by 167 publications

(205 citation statements)

References 34 publications

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“…VUM mx1 belongs to a group of octopamine-immunoreactive neurons (Kreissl et al 1994). Octopamine, a biogenic amine usually associated with increased levels of arousal and behavioral facilitation in invertebrates (Libersat and Pflüger 2004;Huber 2005), had been shown to increase responsiveness of bees to olfactory stimuli (Mercer and Menzel 1982).…”

Section: Neural Bases Of Cs and Us Processingmentioning

confidence: 99%

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

Giurfa

Sandoz²

2012

Learn. Mem.

345

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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Section: Neural Bases Of Cs and Us Processingmentioning

confidence: 99%

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

Giurfa

Sandoz²

2012

Learn. Mem.

345

334

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“…The distribution of octopaminergic neurons is well documented in insects including honeybees, fruit flies, blowflies, cockroaches, hawkmoths, and locusts. [105][106][107][108][109][110][111][112] The best characterized group of neuromodulatory neurons in insects constitutes a unique group of unpaired efferent median neurons, the somata of which are located at the dorsal/ventral midline of the subesophageal ganglion, thoracic, and abdominal ganglia; these neurons are known as dorsal unpaired median or ventral unpaired median neurons. [113][114][115][116] The classification of OCTlike immunoreactive neurons as clusters of cell bodies and perikarya within the cell body in the brain and the subesophageal ganglion has been reviewed elsewhere.…”

Section: Octopaminergic Neurons In the Insect Nervous Systemmentioning

confidence: 99%

“…24,108,109 A subpopulation of the subesophageal ganglion dorsal/ventral unpaired median cells innervates most parts of the brain neuropils and is involved with specific activities and complex behaviors. 105,118 The dorsal unpaired median and ventral unpaired median neurons also innervate sets of peripheral muscles, glands, and certain types of proprioceptors. 119 The peripherally released OCT from dorsal/ ventral unpaired median neurons modulates neuromuscular transmission, muscle contraction kinetics, muscle metabolism, and sensory sensitivity, and influences other properties of target organs.…”

Section: Octopaminergic Neurons In the Insect Nervous Systemmentioning

confidence: 99%

Review of octopamine in insect nervous systems

Farooqui¹

2012

OAIP

145

155

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Octopamine (OCT) belongs to a group of compounds known as biogenic amines. OCT, a monohydroxylic analog of norepinephrine, is found in both vertebrate and invertebrate nervous systems. OCT is present in relatively high concentrations in the neuronal and nonneuronal tissues of most invertebrate species studied. However, OCT occurs as a trace amine in vertebrates where its physiological significance remains uncertain. OCT acts as a neurotransmitter, neuromodulator, and neurohormone in insect nervous systems where it prominently influences multiple physiological events. In the peripheral nervous system, OCT modulates the activity of flight muscles, peripheral organs, and most sense organs. In the central nervous system, OCT is essential for the regulation of motivation, desensitization of sensory inputs, arousal, initiation, and maintenance of various rhythmic behaviors, hygiene behavior, and complex social behaviors, including establishment of labor, as well as learning and memory. As a neurotransmitter, OCT regulates endocrine gland activity and controls the emission of light in the firefly lantern. As a neurohormone, OCT is released into hemolymph, transported to target tissues, and induces mobilization of lipids and carbohydrates, preparing insects for a period of extended activity or assisting recovery from a period of increased energy demand. OCT modulates hemocytic nodulation in nonimmune larvae and enhances phagocytosis as a neurohormone. OCT exerts its effects by binding to specific receptors belonging to the superfamily of G protein-coupled receptors and shares the structural motif of seven transmembrane domains. Activation of octopaminergic receptor types is coupled with different second messenger pathways depending on the species, tissue source, receptor type, and cell line used for expression of the cloned receptor. OCT-mediated generation of second messengers is associated with changes in cellular response, affecting insect behaviors. This review describes the roles of OCT in insect nervous systems at the behavioral and molecular levels.

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“…Kreissl et al (1991) also reported the presence of OA-IR neuronal clusters in median and lateral positions of the antennal lobes of the honeybee, where, according to physiological studies, octopamine is involved in stimulus reinforcement (Bicker and Menzel, 1989).…”

mentioning

confidence: 95%

Octopamine immunoreactivity in the fruit fly Drosophila melanogaster

Monastirioti¹,

Gorczyca²,

Rapus³

et al. 1995

J of Comparative Neurology

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184

170

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Octopamine has been proposed as a neurotransmitter/modulator/hormone serving a variety of physiological functions in invertebrates. We have initiated a study of octopamine in the fruit fly Drosophila melanogaster, which provides an excellent system for genetic and molecular analysis of neuroactive molecules. As a first step, the distribution of octopamine immunoreactivity was studied by means of an octopamine-specific antiserum. We focused on the central nervous system (CNS) and on the innervation of the larval body wall muscles. The larval octopamine neuronal pattern was composed of prominent neurons along the midline of the ventral ganglion, whereas brain lobes were devoid of immunoreactive somata. However, intense immunoreactive neuropil was observed both in the ventral ganglion and in the brain lobes. Some of the immunoreactive neurons sent peripheral fibers that innervated most of the muscles of the larval body wall. Octopamine immunoreactivity was observed at neuromuscular junctions in all larval stages, being present in a well-defined subset of synaptic boutons, type II. Octopamine immunoreactivity in the adult CNS revealed many additional neurons compared to the larval CNS, indicating that at least a subset of adult octopamine neurons may differentiate during metamorphosis. Major octopamineimmunoreactive neuronal clusters and neuronal processes were observed in the subesophageal ganglion, deutocerebrum, and dorsal protocerebrum, and intense neuropil staining was detected primarily in the optic lobes and in the central complex.Keywords octopamine neuron; insect nervous system; neuromuscular junction; synaptic bouton; immunocytochemistry Biogenic amines as chemical messengers in the nervous system of arthropods are thought to play crucial roles in several aspects of their behavior (reviewed by Bicker and Menzel, 1989). Octopamine, one of the biogenic amines extensively studied in invertebrates, has been proposed as neurotransmitter, neuromodulator, and neurohormone in a variety of physiological processes (for reviews, see David and Coulon, 1985;Evans, 1985Evans, , 1992 Address reprint requests to Dr. Maria Monastirioti, Department of Biology, Brandeis University, Waltham, MA 02254.. HHS Public Access Author Manuscript Author ManuscriptAuthor ManuscriptAuthor Manuscript Bicker and Menzel, 1989). In crustaceans, octopamine has been implicated in the neuromodulation of rapid response circuits controlling the escape behavior of crayfish (Glanzman and Krasne, 1983) and in the aggressive and submissive postures in lobsters (reviewed by Kravitz, 1988). In a variety of insect species, octopamine has been implicated in both central and peripheral neural functions. It stimulates activity of the firefly light organ (Nathanson, 1979), induces flight motor activity, and acts as neurotransmitter/modulator in the locust central nervous system (CNS; Sombati and Hoyle, 1984). Octopamine regulates hormone release in cockroaches (Downer et al., 1984), induces lipid and carbohydrate metabolism in crickets (Fields ...

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Octopamine‐like immunoreactivity in the brain and subesophageal ganglion of the honeybee

Cited by 167 publications

References 34 publications

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

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

Review of octopamine in insect nervous systems

Octopamine immunoreactivity in the fruit fly Drosophila melanogaster

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