Effects of Caffeine on Olfactory Learning in Crickets

Abstract

Caffeine is a plant-derived alkaloid that is generally known as a central nervous system (CNS) stimulant. In order to examine the effects of caffeine on higher CNS functions in insects, we used an appetitive olfactory learning paradigm for the cricket Gryllus bimaculatus. Crickets can form significant long-term memories (LTMs) after repetitive training sessions, during which they associate a conditioned stimulus (CS: odor) with an unconditioned stimulus (US: reward). Administration of hemolymphal injections of caffeine established LTM after only single-trial conditioning over a wide range of caffeine dosages (1.6 μ μg/kg to 39 mg/kg). We investigated the physiological mechanisms underlying this enhancement of olfactory learning performance pharmacologically, focusing on three major physiological roles of caffeine: 1) inhibition of phosphodiesterase (PDE), 2) agonism of ryanodine receptors, and 3) antagonism of adenosine receptors. Application of drugs relevant to these actions resulted in significant effects on LTM formation. These results suggest that externally applied caffeine enhances LTM formation in insect olfactory learning via multiple cellular mechanisms.

Roles of Octopamine and Dopamine Neurons for Mediating Appetitive and Aversive Signals in Pavlovian Conditioning in Crickets

“…They also exhibit excellent capability to learn color and pattern of visual targets (Unoki et al, 2006 ; Nakatani et al, 2009 ; Matsumoto et al, 2013b ). Second, applications of pharmacological studies (Unoki et al, 2005 , 2006 ; Matsumoto et al, 2006 , 2016 ; Matsumoto Y. et al, 2009 ; Mizunami et al, 2014 ; Sugimachi et al, 2016 ), gene knockdown by RNA interference (RNAi; Takahashi et al, 2009 ; Awata et al, 2016 ), and genome editing by the CRISPR/Cas9 system (Awata et al, 2015 ) are feasible, thereby greatly facilitating the analysis of molecular basis of learning and memory. Indeed, it can be stated that crickets are one of the best insect models for pharmacological analysis of learning and memory (Mizunami et al, 2013 ).…”

Anatabine ameliorates intestinal inflammation and reduces the production of pro-inflammatory factors in a dextran sulfate sodium mouse model of colitis

“…Strikingly, our findings suggested that factors contributing to anatabine-associated reduction of GPCR cascades included a wide range of cyclic nucleotide phosphodiesterases (PDEs) —including several subtypes of PDE1, PDE3, PDE4, PDE7, PDE8, and PDE10—which modulate the intracellular concentrations of cAMP and cyclic guanosine monophosphate (cGMP) by regulating their rates of degradation [ 67 ]. In this regard, several naturally occurring alkaloids, such as caffeine and tolafentrine, also inhibit PDE activities [ 68 , 69 ]. The opium alkaloid papaverine has been identified as a potent and specific inhibitor of PDE10A, with the ability to trigger cAMP and cGMP accumulation as well as CREB phosphorylation in several animal behavioral models [ 70 , 71 ].…”

Limited evidence for learning in a shuttle box paradigm in crickets (Acheta domesticus)

“…G. bimaculatus has also been shown to have good olfactory memory, with some associations being remembered for at least six weeks (Matsumoto and Mizunami 2002). Other work on memory in G. bimaculatus has shown that caffeine can improve long-term memory in this species (Sugimachi et al 2016).…”