Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology

Abstract

Abstract. The biogenic amines serotonin (5HT) and octopamine (OA) exist in the bee and can modulate neuronal activity and behaviour. 5HT-like and OA-like immunoreactivities can be found in most neuropils of the brain. Binding sites for the two amines are also present in most brain neuropils. The highest density of binding sites for [3H]serotonin and [3H]octopamine was found in the mushroom bodies. In some brain areas, especially the mushroom bodies, mismatches exist between binding sites and immunoreactivities, suggesting that the two amines also bind to neuropils which are not directly innervated by 5HT-like or OA-like immunoreactive neurons. The action of the two amines on behaviour in the bee is antagonistic. In the antennal pathway, proboscis and antennal responses to olfactory and gustatory stimuli are enhanced by OA and reduced by 5HT. In olfactory conditioning experiments, storage and retrieval of the learned signal can be enhanced by OA and reduced by 5HT. The specificity of these effects depends on the site of amine application in the neuropil. In the visual system the direction specificity of the visual antennal response is enhanced by OA and reduced by 5HT after topical application or injection into the lobula, the third optic ganglion. Correlates for the behavioural modulation can be found in higher-order visual interneurons. While OA application can mimic the stimulation of the bee with sugar water, the behavioural conditions leading to the release of 5HT are not yet known.Key words. Insect; honey bee; behaviour; neuromodulation; serotonin; octopamine. IntroduetionAnimals have to cope with~unpredictable and changing environmental conditions. They have to find food, territories, and partners; they have to escape enemies and environmental threats. The appropriate behaviours to solve these problems are initiated and controlled by the brain which has the vital task of determining, sometimes within fractions of a second, the best response to a given constellation of inputs. Neurobiological research on arthopods has shown that nervous systems can solve these adaptive tasks by modulating the properties of sensory cells, nerve cells and even muscles 1,5,28. This modulation of single network elements can in turn change the properties of the whole network and consequently can modify behaviour 5. We have chosen the honeybee to study these questions because the behaviour, neuroanatomy and physiology of this insect have been analysed in great detail by generations of biologists. Behavioural analyses using stereotyped and adaptive behaviours can be performed under controlled laboratory conditions and it is possible to attribute specific behavioural functions to parts of the bee's nervous system 21"24,55. Research in the last few years has shown that biogenic amines, which are present in the bee nervous system, play an important role in behavioural modulation in other animal groups 5. The analyses of the processes by which biogenic amines modify behaviour in the bee therefore have significance for other nervous sys...

Octopamine modulates honey bee dance behavior

“…Consequently, it will be interesting to clarify whether dopamine and OA indeed have similar effects on dance behavior. Serotonin has also been shown to act in opposition to OA in sensory systems (25)(26)(27), and it is an important modulator of the visual system (26); however, whether it modulates dance behavior is presently unknown.…”

“…OA is known to increase sensitivity and responsiveness to sucrose (17,23,25). In studies of associative learning, OA modulates the learning of sucrose reward in honey bees and Drosophila melanogaster (22,24,28) and may represent the sucrose unconditioned stimulus in the bee brain (29), i.e., the neurochemical released by the perception of sucrose that modulates downstream behavioral responses.…”

Octopamine and Experience-Dependent Modulation of Aggression in Crickets

“…Hence, serotonin invokes lobsters to adopt an aggressive posture (Harris-Warrick and Kravitz, 1984;Harris-Warrick, 1985) and increases the willingness to fight while reducing the tendency to withdraw (Huber et al, 1997a;Huber and Delago, 1998). On the other hand, octopamine, the phenol analog of noradrenaline (for review, see Evans, 1985;Roeder, 1999) and a behavioral antagonist to serotonin in many invertebrate systems (for review, see Bicker and Menzel, 1989;Erber et al, 1993), causes crustaceans to adopt a submissive body posture (Livingstone et al, 1980;Antonsen and Paul, 1997).…”

Dietary dopamine causes ovary activation in queenless Apis mellifera workers

“…Biogenic amines in the central nervous system, especially dopamine, octopamine and serotonin, are candidates to respond to variations in queen pheromone. By functioning as neurotransmitters, neuromodulators and neurohormones (Bicker and Menzel, 1989;Roeder, 1994;Osborne, 1996) the biogenic amines modulate a diversity of physiological and behavioral functions in honey bees, such as learning and olfactory memory (Bicker and Menzel, 1989;Erber et al, 1993;Menzel and Müller, 1996;Blenau et al, 1998), recruitment behavior (Bozic and Woodring, 1998), age-related division of labor (Taylor et al, 1992;Robinson, 1999, 2001;Wagener-Hulme et al, 1999), nestmate recognition , foraging behavior (Barron et al, 2002), and changes in morphological development (Taylor et al, 1992). Also, in honey bees, as well as in the bumble bee Bombus terrestris L., high levels of dopamine in the brain correlate with physiologically active ovaries and fully developed oocytes (Harris and Woodring, 1995;Bloch et al, 2000;Sasaki and Nagao, 2001).…”