Habituation of an appetitive reflex in the honeybee

Abstract

1. The proboscis extension reflex is an appetitive component of the bee's feeding behavior that is elicited by touching one antenna with a droplet of sugar water. Repetitive stimulation leads to a decrement and finally to the disappearance of the response, which can be restored by stimulating the contralateral antenna. This behavioral plasticity conforms to essential parametric characteristics for habituation. 2. The response was quantified by recording extracellularly from a muscle involved in proboscis movement, by measuring the duration of the proboscis extension, or by determining the number of trials necessary to abolish any visible response. 3. Because habituation was restricted to the repetitively stimulated antenna and did not generalize to the contralateral hemisphere, the neural circuits mediating habituation may be confined to one hemisphere. 4. State dependence of habituation could be demonstrated by showing that hungry animals exhibited a smaller response decrement and required more trials until disappearance of the response compared with satiated animals. The initial response and the subsequent response decrement are separate components determined by satiation level and stimulus strength. 5. Depleting the nervous system of monoamines by the use of reserpine abolished the reflex in 30% of the animals and reduced responsiveness in the remainder. Injection of octopamine or its metabolic precursor tyramine restored the reflex in reserpinized unresponsive animals, and tyramine also enhanced the muscle-spike discharge of reserpinized, responsive animals. In undepleted animals, tyramine application also accelerated the rate of habituation of the reflex. We therefore propose that octopaminergic neurons participate in mediating food arousal and the state dependence of habituation and, in a separate process, influence the response decrement during habituation. 6. Application of an acetylcholine esterase (AChE) inhibitor and a cholinergic receptor blocker confirmed histochemical data that implicate cholinergic transmission in the reflex pathways. 7. The combined pharmacological dissection of the reflex and immunocytochemical investigations of its chemical architecture provide evidence that the proboscis extension reflex is mediated by nonaminergic and monoaminergic pathways operating in parallel.

Side-Specificity of Olfactory Learning in the Honeybee: US Input Side

“…This indicates that the compound-US induces two processes, a unilateral antenna-US process, and a bilateral proboscis-US process. The fact that sensitization after an antenna-US is lateralized is particularly interesting, because another nonassociative learning phenomenon, habituation, was already found to be limited to the stimulated side (Braun and Bicker 1992). After habituation, however, a strong stimulation on the opposite side dishabituates the reflex, indicating some cross-talk of US pathways between brain sides with respect to nonassociative plasticity.…”

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

“…In contrast to the retardation experiment, a multiple-trial procedure was used to rule out the possibility that backward inhibitory learning is only a single-trial effect. To allow for a graded measure of the PER, electromyogram recordings were taken from muscle M17, which monitors the whole PER and was used for measuring experience-dependent changes of the motor program underlying PER (Rehder 1987;Smith and Menzel 1989;Braun and Bicker 1992;Hammer et al 1994). …”

Characterization of a tyramine receptor from Caenorhabditis elegans

“…The biosynthesis of OA requires the hydroxylation of tyramine (TA) to OA by tyramine b-hydroxylase and the effects of OA and TA are mediated by G-protein coupled receptors, many of which positively or negatively modulate adenylyl cyclase activity (Roeder 1999). Studies on the physiological role and signaling of OA and its precursor TA have focused largely on insects where, OA and TA regulate a variety of processes, including energy generation via fat body metabolism (Downer 1979;Wang et al 1990;Blau and Wegener 1994;Park and Keeley 1998), regulation of egg-laying (Monastirioti et al 1996;Torfs et al 2000) and induction of feeding (Braun and Bicker 1992). The role of TA and OA in mammals is not well studied but has recently gained much attention due to the isolation of human and rodent receptors that specifically bind TA and couple to G as , highlighting the need to re-evaluate the role of these trace amines in vertebrates (Borowsky et al 2001).…”