Cocaine affects foraging behaviour and biogenic amine modulated behavioural reflexes in honey bees

Abstract

In humans and other mammals, drugs of abuse alter the function of biogenic amine pathways in the brain leading to the subjective experience of reward and euphoria. Biogenic amine pathways are involved in reward processing across diverse animal phyla, however whether cocaine acts on these neurochemical pathways to cause similar rewarding behavioural effects in animal phyla other than mammals is unclear. Previously, it has been shown that bees are more likely to dance (a signal of perceived reward) when returning from a sucrose feeder after cocaine treatment. Here we examined more broadly whether cocaine altered reward-related behaviour, and biogenic amine modulated behavioural responses in bees. Bees developed a preference for locations at which they received cocaine, and when foraging at low quality sucrose feeders increase their foraging rate in response to cocaine treatment. Cocaine also increased reflexive proboscis extension to sucrose, and sting extension to electric shock. Both of these simple reflexes are modulated by biogenic amines. This shows that systemic cocaine treatment alters behavioural responses that are modulated by biogenic amines in insects. Since insect reward responses involve both octopamine and dopamine signalling, we conclude that cocaine treatment altered diverse reward-related aspects of behaviour in bees. We discuss the implications of these results for understanding the ecology of cocaine as a plant defence compound. Our findings further validate the honey bee as a model system for understanding the behavioural impacts of cocaine, and potentially other drugs of abuse.

Keywords: Addiction; Cocaine; Dopamine; Drug reward; Honey bee; Invertebrate neuroscience; Reward systems.

Figure 1. Schematic of experimental set-up used for foraging preference experiment.

In the foraging preference experiment, bees were trained to two tunnels. One was blue with vertical stripes while the other was green with horizontal stripes. The difference between the two tunnels was to make it as easy as possible for the bees to tell the two tunnels apart.

Figure 2. Foraging behaviour in honey bees following cocaine administration.

(A) Scatter plot showing the effect of topical cocaine treatment on preference for the green arm. Each point represents one bee. Dotted lines mark median values for each treatment group. The preference for the green arm was significantly higher for cocaine-treated than control-treated bees (Mann–Witney U = 2, 185, p = 0.0038). (B) Effect of volatilised cocaine treatment on visitation rate at a sucrose feeder (error bars represent standard error). Bees treated with volatilised cocaine (grey bars) increased their rate of foraging relative to controls (white bars) when foraging at a 0.5 M sucrose feeder (t₇₀ = 5.0710, p = 0.00003), but not at a 2 M sucrose feeder (t₇₀ = −0.2087, p = 0.8353).

Figure 3. Behavioural responsiveness following cocaine administration in honey bees.

(A) Proportion of bees responding to 10% sucrose following treatment with 0 or 10 µg of volatilised cocaine (error bars represents standard error and letters denote statistically different groups). There was a significant increase in sucrose responsiveness in bees treated with 10 µg cocaine relative to control (χ² = 6.1013, df = 1, p = 0.0135). (B) Proportion of bees responding to 10% sucrose following treatment with 0, 5, 10, 20, or 50 µg of volatilised cocaine. There was a dose-dependent relationship between cocaine dose and sucrose responsiveness (χ² = 14.089, df = 4, p = 0.0070). (C) Shock responsiveness of bees following cocaine administration. Curves are based on weibull distributions of shock responsiveness for each group. Comparisons are based on estimates of EV₅₀ for 40 bees per group (F_4,40 = 5.4, p = 0.0015). Pairwise comparisons found that the 50 µg group was different from all other groups, while the remaining cocaine treated groups were different from controls.