Steroid hormone (20-hydroxyecdysone) modulates the acquisition of aversive olfactory memories in pollen forager honeybees

Abstract

Here, we examine effects of the steroid hormone, 20-hydroxyecdysone (20-E), on associative olfactory learning in the honeybee, Apis mellifera. 20-E impaired the bees' ability to associate odors with punishment during aversive conditioning, but did not interfere with their ability to associate odors with a food reward (appetitive learning). The steroid had a significant impact also on the expression of amine-receptor genes in centers of the brain involved in the formation and recall of associative olfactory memories (mushroom bodies). 20-E increased expression of the dopamine receptor gene, Amdop2, and reduced the expression of the putative dopamine/ecdysone receptor gene, Amgpcr19. Interestingly, Amgpcr19 tended to be highly expressed in the brains of foragers that exhibited strong aversive learning, but expressed at lower levels in bees that performed well in appetitive learning assays. In 2-d-old bees, transcript levels of the same gene could be reduced by queen mandibular pheromone, a pheromone that blocks aversive learning in young worker bees. As ecdysteroid levels rise to a peak 2 d after adult emergence and then fall to low levels in foragers, we examined aversive learning also in young worker bees. Aversive learning performance in 2-d-old bees was consistently poor. The results of this study indicate that learning in honeybees can be modulated by ecdysteroids. They highlight, in addition, a potential involvement of the putative dopamine/ecdysone receptor, AmGPCR19, in hormonal regulation of associative olfactory learning in the honeybee.

Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae

“…The discovery that male-transferred 20E is a key regulator of female reproductive biology in An. gambiae adds to the myriad of effects that this hormone exerts on insect adult physiology (2,3,(17)(18)(19)(20)(21)(22)(23). Interestingly, the steady decline of 20E levels in the atrium during the first day after copulation (17) is reminiscent of the process of mating plug digestion, which is completed in a similar time frame (5)(6)(7)16).…”

“…This hormone has been found to affect multiple aspects of adult insect physiology: It controls lifespan (19), learning (20), stress-induced responses (21), sleep regulation, and social interactions (22). Moreover 20E acts as a sexual hormone, influencing male sexual behavior in Drosophila (23).…”

Rules and mechanisms of punishment learning in honey bees: the aversive conditioning of the sting extension response

“…The lack of specific pharmacological blockers of these receptors has until now precluded straightforward analyses of their role in aversive learning. Impairment of aversive learning yields conflicting evidence with respect to this topic: while pharmacological blocking with vertebrate antagonists indicated that AmDOP2 receptors are necessary for aversive learning (Vergoz et al, 2007a), analyses of transcript levels of dopaminergic receptor genes suggested that impairment of aversive learning is associated with an increase of AmDOP2 receptors (Geddes et al, 2013). More experiments are necessary to elucidate whether and how these different receptors contribute to aversive learning.…”

“…An interesting twist to the study of aversive learning and dopaminergic signaling is the discovery that 20-hydroxyecdisone (20E), a metabolite of the steroid hormone ecdysone, which intervenes in insect development and reproduction (Riddiford et al, 2000), impairs aversive but not appetitive conditioning in bees (Geddes et al, 2013). This impairment seems to be achieved in part via the dopamine/ecdysone receptor gene AmGPCR19, which is the honeybee ortholog of the dopamine/ecdysone receptor gene 48 (DmDopEcR) identified in Drosophila (Srivastava et al, 2005).…”

Effects of Caffeine on Olfactory Learning in Crickets

“…Insects, the most diverse group of invertebrates, also serve as useful models for studying higher CNS functions because of the simplicity of their nervous system, their amenability to genetic approaches, and the availability of established learning paradigms (Heisenberg, 2003;Mizunami et al, 2004;Giurfa, 2013). The best-known experimental paradigm for learning and memory in insects is olfactory associative conditioning in honeybees, in which bees associate a specific odor presented as a CS in a training session, with a reward (usually sucrose solution) presented as a US (Takeda, 1961;Bitterman et al, 1983;Menzel, 2012;Geddes et al, 2013;Scheiner et al, 2013). Since honeybees have the most prominent learning and memory capacity among insect species, this paradigm has frequently been used as a model system to explore their behavioral and physiological mechanisms (Sandoz, 2011;Menzel, 2012;Scheiner et al, 2013).…”