Salivary Digestion Extends the Range of Sugar-Aversions in the German Cockroach

Saliva has diverse functions in feeding behavior of animals. However, the impact of salivary digestion of food on insect gustatory information processing is poorly documented. Glucose-aversion (GA) in the German cockroach, Blattella germanica, is a highly adaptive heritable behavioral resistance trait that protects the cockroach from ingesting glucose-containing-insecticide-baits. In this study, we confirmed that GA cockroaches rejected glucose, but they accepted oligosaccharides. However, whereas wild-type cockroaches that accepted glucose also satiated on oligosaccharides, GA cockroaches ceased ingesting the oligosaccharides within seconds, resulting in significantly lower consumption. We hypothesized that saliva might hydrolyze oligosaccharides, releasing glucose and terminating feeding. By mixing artificially collected cockroach saliva with various oligosaccharides, we demonstrated oligosaccharide-aversion in GA cockroaches. Acarbose, an alpha-glucosidase inhibitor, prevented the accumulation of glucose and rescued the phagostimulatory response and ingestion of oligosaccharides. Our results indicate that pre-oral and oral hydrolysis of oligosaccharides by salivary alpha-glucosidases released glucose, which was then processed by the gustatory system of GA cockroaches as a deterrent and caused the rejection of food. We suggest that the genetic mechanism of glucose-aversion support an extended aversion phenotype that includes glucose-containing oligosaccharides. Salivary digestion protects the cockroach from ingesting toxic chemicals and thus could support the rapid evolution of behavioral and physiological resistance in cockroach populations.

Salivary Digestion Extends the Range of Sugar-Aversions in the German Cockroach

Saliva has diverse functions in feeding behavior of animals. However, the impact of salivary digestion of food on insect gustatory information processing is poorly documented. Glucose-aversion (GA) in the German cockroach, Blattella germanica, is a highly adaptive heritable behavioral resistance trait that protects the cockroach from ingesting glucose-containing-insecticide-baits. In this study, we confirmed that GA cockroaches rejected glucose, but they accepted oligosaccharides. However, whereas wild-type cockroaches that accepted glucose also satiated on oligosaccharides, GA cockroaches ceased ingesting the oligosaccharides within seconds, resulting in significantly lower consumption. We hypothesized that saliva might hydrolyze oligosaccharides, releasing glucose and terminating feeding. By mixing artificially collected cockroach saliva with various oligosaccharides, we demonstrated oligosaccharide-aversion in GA cockroaches. Acarbose, an alpha-glucosidase inhibitor, prevented the accumulation of glucose and rescued the phagostimulatory response and ingestion of oligosaccharides. Our results indicate that pre-oral and oral hydrolysis of oligosaccharides by salivary alpha-glucosidases released glucose, which was then processed by the gustatory system of GA cockroaches as a deterrent and caused the rejection of food. We suggest that the genetic mechanism of glucose-aversion support an extended aversion phenotype that includes glucose-containing oligosaccharides. Salivary digestion protects the cockroach from ingesting toxic chemicals and thus could support the rapid evolution of behavioral and physiological resistance in cockroach populations.

Distributed Representation of Taste Quality by Second-Order Gustatory Neurons in Drosophila

SUMMARYSweet and bitter compounds excite different sensory cells and drive opposing behaviors. It is commonly thought that the neural circuits linking taste sensation to behavior conform to a labeled-line architecture, but in Drosophila, evidence for labeled lines beyond first-order neurons is lacking. To address this, we devised trans-Tango(activity), a strategy for calcium imaging of second-order gustatory projection neurons based on trans-Tango, a genetic transsynaptic tracing technique. We found distinct projection neuron populations that respond to sweet and bitter tastants. However, the bitter-responsive population was also activated by water alone. We further discovered that bitter tastants evoke activity upon both stimulus onset and offset. Bitter offset responses are exhibited by both first- and second-order gustatory neurons, but these responses are distributed among multiple types of projection neurons in the second order. These findings suggest a more complex coding scheme for gustatory information than can be explained by a labeled line model.

Mechanosensory circuits coordinate two opposing motor actions in Drosophila feeding

Mechanoreception detects physical forces in the senses of hearing, touch, and proprioception. Here, we show that labellar mechanoreception wires two motor circuits to facilitate and terminate Drosophila feeding. Using patch-clamp recordings, we identified mechanosensory neurons (MSNs) in taste pegs of the inner labella and taste bristles of the outer labella, both of which rely on the same mechanoreceptor, NOMPC (no mechanoreceptor potential C), to transduce mechanical deflection. Connecting with distinct brain motor circuits, bristle MSNs drive labellar spread to facilitate feeding and peg MSNs elicit proboscis retraction to terminate feeding. Bitter sense modulates these two mechanosensory circuits in opposing manners, preventing labellar spread by bristle MSNs and promoting proboscis retraction by peg MSNs. Together, these labeled-line circuits enable labellar peg and bristle MSNs to use the same mechanoreceptors to direct opposing feeding actions and differentially integrate gustatory information in shaping feeding decisions.

Modulation of taste processing by temperature

Taste stimuli have a temperature that can stimulate thermosensitive neural machinery in the mouth during gustatory experience. Although taste and oral temperature are sometimes discussed as different oral sensory modalities, there is a body of literature that demonstrates temperature is an important component and modulator of the intensity of gustatory neural and perceptual responses. Available data indicate that the influence of temperature on taste, herein referred to as “thermogustation,” can vary across taste qualities, can also vary among stimuli presumed to share a common taste quality, and is conditioned on taste stimulus concentration, with neuronal and psychophysical data revealing larger modulatory effects of temperature on gustatory responding to weakened taste solutions compared with concentrated. What is more, thermogustation is evidenced to involve interplay between mouth and stimulus temperature. Given these and other dependencies, identifying principles by which thermal input affects gustatory information flow in the nervous system may be important for ultimately unravelling the organization of neural circuits for taste and defining their involvement with multisensory processing related to flavor. Yet thermal effects are relatively understudied in gustatory neuroscience. Major gaps in our understanding of the mechanisms and consequences of thermogustation include delineating supporting receptors, the potential involvement of oral thermal and somatosensory trigeminal neurons in thermogustatory interactions, and the broader operational roles of temperature in gustatory processing. This review will discuss these and other issues in the context of the literature relevant to understanding thermogustation.

Identification of single pair of interneurons for bitter taste processing in the Drosophila brain

ABSTRACTDrosophila has become an excellent model system for investigating the organization and function of the gustatory system due to the relatively simple neuroanatomical organization of its brain and the availability of powerful genetic and transgenic technology. Thus, at the molecular and cellular level, a great deal of insight into the peripheral detection and coding of gustatory information has already been attained. In contrast, much less is known about the central neural circuits that process this information and induce behaviorally appropriate motor output. Here we combine functional behavioral tests with targeted transgene expression through specific driver lines to identify a single bilaterally homologous pair of bitter sensitive interneurons that are located in the subesophageal zone of the brain. Anatomical and functional data indicate that these interneurons receive specific synaptic input from bitter sensitive gustatory receptor neurons. Targeted transgenic activation and inactivation experiments show that these bitter sensitive interneurons can largely suppress the proboscis extension reflex to appetitive stimuli such as sugar and water. These functional experiments together with calcium-imaging studies indicate that these first order local interneurons play an important role in the inhibition of the proboscis extension reflex that occurs in response to bitter tastants. Taken together, our studies present a cellular identification and functional characterization of a key gustatory interneuron in the bitter sensitive gustatory circuitry of the adult fly.