Pharmacological modulation of aversive responsiveness in honey bees

Stevanus R Tedjakumala,Martin Giurfa,Margaux Aimable

doi:10.3389/fnbeh.2013.00221

Abstract

Within a honey bee colony, individuals performing different tasks exhibit different sensitivities to noxious stimuli. Noxious-stimulus sensitivity can be quantified in harnessed bees by measuring the sting extension response (SER) to a series of increasing voltages. Biogenic amines play a crucial role in the control of insect responsiveness. Whether or not these neurotransmitters affect the central control of aversive responsiveness, and more specifically of electric-shock responsiveness, remains unknown. Here we studied the involvement of the biogenic amines octopamine, dopamine and serotonin, and of the ecdysteroid 20-hydroxyecdisone in the central control of sting responsiveness to electric shocks. We injected pharmacological antagonists of these signaling pathways into the brain of harnessed bees and determined the effect of blocking these different forms of neurotransmission on shock responsiveness. We found that both octopamine and 20-hydroxyecdisone are dispensable for shock responsiveness while dopamine and serotonin act as down-regulators of sting responsiveness. As a consequence, antagonists of these two biogenic amines induce an increase in shock responsiveness to shocks of intermediate voltage; serotonin, can also increase non-specific responsiveness. We suggest that different classes of dopaminergic neurons exist in the bee brain and we define at least two categories: an instructive class mediating aversive labeling of conditioned stimuli in associative learning, and a global gain-control class which down-regulates responsiveness upon perception of noxious stimuli. Serotonergic signaling together with down-regulating dopaminergic signaling may play an essential role in attentional processes by suppressing responses to irrelevant, non-predictive stimuli, thereby allowing efficient behavioral performances.

Highlights

Honey bees are a well-established model for the study of learning and memory (Menzel, 1999; Giurfa, 2007)
The differential effect of these two methiothepin concentrations on shock responsiveness shows that our experiments were done at reasonably moderate drugs concentrations, so that the enhancing effect induced by higher methiothepin concentrations was through blockade of 5-HT receptors
Our study provides the first neuropharmacological dissection of the neurotransmitter systems underlying the central control of sting responsiveness to noxious stimuli in honey bees

Summary

Introduction

Honey bees are a well-established model for the study of learning and memory (Menzel, 1999; Giurfa, 2007). Associative olfactory learning is studied using harnessed bees subjected to Pavlovian protocols such as the appetitive conditioning of the proboscis extension reflex (PER) (Takeda, 1961; Bitterman et al, 1983; Giurfa and Sandoz, 2012) and the aversive conditioning of the sting extension reflex (SER)(Vergoz et al, 2007; Carcaud et al, 2009; Giurfa et al, 2009) In the former, bees learn to associate an odorant as conditioned stimulus (CS) with sucrose solution as unconditioned stimulus (US). They show that sensitivity to noxious stimulations may determine behavioral biases and specializations within the hive, contributing to the social organization of the colony (Roussel et al, 2009; Tedjakumala and Giurfa, 2013)

Methods

Results

Conclusion