Behavioral and electrophysiological studies of glucose-aversive behavior in the German cockroach

Glucose is a universal phagostimulant in many animal species. However, some populations of the German cockroach are behaviorally deterred from eating glucose. It is thought that the “glucose-aversion” trait has evolved in response to toxic baits containing glucose. To understand the mechanisms that underlie glucose-aversion, we focused on 1) identifying the gustatory organs involved in the glucose-averse behavior, and 2) characterizing the electrophysiological responses of gustatory neurons to glucose and other tastants, such as fructose and caffeine. In two-choice feeding assays, the glucose-averse cockroaches consumed fructose but not glucose or caffeine. In cockroaches with intact paraglossa, but with ablated maxillary and labial palps, water drinking behavior was inhibited by increasing concentrations of glucose. Moreover, adding glucose to both fructose and caffeine reduced feeding responses. In electrophysiological recordings from sensilla on the paraglossa of normal cockroaches, glucose and fructose elicited neural responses from the sweet taste receptor neuron (sugar receptor cell) involved in evoking feeding behavior. Caffeine elicited responses from the bitter taste receptor neuron (bitter receptor cell). On the other hand, while fructose also elicited responses from the sugar cell in the glucose-averse cockroaches, glucose elicited neural responses from both the sugar and bitter receptor cells. Generally, activation of bitter receptor cells suppresses feeding behavior and evokes aversive behaviors in animals. Our results indicate that glucose can be received as both sweet and bitter tastants at the peripheral sensory level of glucose-averse cockroaches. We hypothesize that in the glucose-averse cockroaches, components of the glucose reception system are atypically expressed on the bitter receptor cells, thus deterring feeding responses to glucose.