Three Drosophila mutations that block associative learning also affect habituation and sensitization.

Abstract

Drosophila melanogaster has been conditioned with shock to avoid various odors. Mutants that failed to learn this task have been isolated. Here we report tests on these mutants for more elementary types of behavioral plasticity-habituation and sensitization of a reflex. Fruit flies have taste receptors on their feet. When a starved, water-satiated fly has sucrose applied to one foot, it usually responds by extending its proboscis. In normal flies this feeding reflex shows habituation: application of sugar to one foot depresses responsiveness through the contralateral leg for at least 10 min. The reflex also shows brief sensitization: application of concentrated sucrose solution to the proboscis increases subsequent responsiveness to tarsal stimulation for 2-5 min. In three associative learning mutants, the proboscis-extension reflex is present with a normal threshold but behavioral modulation of the response is altered. The dunce, turnip, and rutabaga mutants all habituate less than normal flies. In addition, sensitization wanes unusually rapidly in dunce and rutabaga flies, lasting less than a minute in the case of dunce.Animals can modify their behavior, based on past experience, in several ways. Along with associative learning, which includes classical and operant conditioning, they show two elementary types of neurally mediated behavioral plasticity which may be considered forms of nonassociative learning. Habituation, broadly defined, is the decrease in a behavioral response on repeated presentations of the same stimulus. (If the decrease merely reflects a change in the sensory receptors it is called "adaptation.") Sensitization, on the other hand, is an increase in an animal's responsiveness after a strong or novel stimulus. Whether habituation, sensitization, and learning rely on similar neural mechanisms is currently not known. This issue has recently become important.Associative learning corresponds to "learning" used in the educational sense, and psychological research has concentrated on this phenomenon. Nevertheless, progress in understanding the underlying mechanism has been slow. The physical and chemical changes that take place when an associative memory is stored in the brain are not known.By contrast, habituation and sensitization look relatively uncomplicated and seem to be amenable to elucidation with present techniques. Recently, in fact, there has been rapid progress in this area. In particular Kandel and his colleagues (1-3) working with the mollusc Aplysia, have found that a gill-withdrawal reflex undergoes habituation and sensitization. They have been able to correlate this behavioral plasticity with changing transmission efficacy in a few parallel synapses in the central nervous system, and they have identified physiological and biochemical events that appear to underlie the synaptic changes. The general applicability of their model has not been established. It is unlikely, for example, that habituation proceeds by the same mechanism in all cases. Nevertheless, other workers (4-...

Operant conditioning in invertebrates

“…Research on the genetically renowned fruit fly Drosophila (Figure 1a) has been revealing a steady flow of genes that are involved in olfactory classical conditioning for the past three decades [3][4][5][6][7][8][9][10][11]. Many of these genes affect the level of the second-messenger cAMP and are preferentially expressed in a prominent neuropil in the fly's brain, the mushroom bodies (Figure 1b; [12][13][14]).…”

Conservation of gene function in behaviour

“…Another is sensitization, an increase in response to a neutral stimulus following exposure to a stronger stimulus. Habituation and sensitization are observed in species as diverse as C. elegans [55], D. melanogaster [56], Rattus norvegicus [57] and humans [58]. Associative learning has also been observed in many species [59,60].…”

Isolation of the Drosophila melanogaster dunce chromosomal region and recombinational mapping of dunce sequences with restriction site polymorphisms as genetic markers.

“…In addition, dnc mutations disrupt one aspect of normal courtship behavior (13). Although normal learning by dnc mutants is not detected in some situations (11), the mutants learn normally but forget rapidly in others (8,10,31). Consequently, dnc flies are best classed as memory mutants. The observation that the dnc mutation perturbs normal cyclic AMP metabolism (4) led to the suggestion that cyclic AMP is intimately involved in behavioral plasticity, a conclusion also reached frotn studies of learning and memory by Aplysia (15).…”

“…In addition, dnc mutations disrupt one aspect of normal courtship behavior (13). Although normal learning by dnc mutants is not detected in some situations (11), the mutants learn normally but forget rapidly in others (8,10,31). Consequently, dnc flies are best classed as memory mutants.…”

“…The associative learning deficit is manifest not only in flies but also in dnc mutant larvae (1). Operant conditioning is altered by lesions in this gene (3), as are the nonassociative learning responses of habituation and sensitization (10). In addition, dnc mutations disrupt one aspect of normal courtship behavior (13).…”