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, 21 (9), 746-50

Remembering Nutrient Quality of Sugar in Drosophila

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Remembering Nutrient Quality of Sugar in Drosophila

Christopher J Burke et al. Curr Biol.

Abstract

Taste is an early stage in food and drink selection for most animals [1, 2]. Detecting sweetness indicates the presence of sugar and possible caloric content. However, sweet taste can be an unreliable predictor of nutrient value because some sugars cannot be metabolized. In addition, discrete sugars are detected by the same sensory neurons in the mammalian [3] and insect [4, 5] gustatory systems, making it difficult for animals to readily distinguish the identity of different sugars using taste alone [6-8]. Here we used an appetitive memory assay in Drosophila [9-11] to investigate the contribution of palatability and relative nutritional value of sugars to memory formation. We show that palatability and nutrient value both contribute to reinforcement of appetitive memory. Nonnutritious sugars formed less robust memory that could be augmented by supplementing with a tasteless but nutritious substance. Nutrient information is conveyed to the brain within minutes of training, when it can be used to guide expression of a sugar-preference memory. Therefore, flies can rapidly learn to discriminate between sugars using a postingestive reward evaluation system, and they preferentially remember nutritious sugars.

Figures

Figure 1
Figure 1. Fruit flies conditioned with palatable and nutritious sugars form robust persistent memory
(A) Sucrose and fructose support fruit fly survival for several days but xylose and arabinose do not. Survival on fructose or sucrose was statistically different from water (1% agar) at all time points after 24hr. Xylose was not statistically different to water (all p>0.13) except at 84hr (p=0.04). Arabinose was statistically different to water at all time points after 24hr (all p<0.01, T-test). All sugars were 3M in 1% agar. Data are mean ± standard error of the mean (SEM). n=10 for each data point. (B) Sucrose, fructose, arabinose and to a lesser extent xylose, elicit proboscis extension behavior. Flies were presented with all sugars as 3M solutions to the front leg. Performance of xylose exposed flies is statistically different from all other groups (all p<0.01, chi-squared test, marked by asterisk). n≥20 flies for each sugar. (C) Short-term appetitive memory following conditioning with sucrose, fructose, arabinose and xylose. Performance of sucrose conditioned flies is statistically different from arabinose and xylose conditioned flies (both p<0.01 and p<0.005). Arabinose performance is also statistically different to xylose (p<0.04, ANOVA). Data are mean ± SEM. n≥14 except xylose n=6. (D) Sucrose and fructose form robust 24hr memory but arabinose and xylose do not. Asterisks denote significant difference between marked groups and all others (all p<0.01). There is no statistical difference between arabinose and xylose performance (p=0.6, ANOVA). Data are mean ± SEM. n≥16. (E) A similar amount of each dyed sugar is consumed during a 5min mock training session. Each sugar was mixed with dye and presented dried on filter paper in the conditioning apparatus. No statistical differences were observed between sugars (all p>0.05, ANOVA) although all were statistically different to dye alone (water, p<0.01). Data are mean ± SEM. n≥8.
Figure 2
Figure 2. Olfactory conditioning with arabinose or xylose supplemented with nutritious sorbitol forms robust 24hr memory
(A) Sorbitol, maltodextrin and sucrose support fruit fly survival for several days. The number of flies alive on sorbitol or maltodextrin was statistically indistinguishable to those on sucrose at all time points (p>0.07) except at 84hr where maltodextrin was different to sucrose (p=0.03, asterisk). Survival on sorbitol, maltodextrin and sucrose was statistically different to on water at all time points (all p<0.01). Data are mean ± SEM. n=10 for each data point. (B) Sucrose and maltodextrin elicit robust proboscis extension behavior but sorbitol does not. Flies were presented with 3M solutions of sucrose or sorbitol or 1.25M maltodextrin to the front leg. Performance of sorbitol exposed flies is statistically different from other groups (p<0.01, chi-squared test, marked by asterisk). n≥20 flies for each sugar. (C) Training with sorbitol supplemented arabinose forms persistent memory. 24hr appetitive memory performance of flies trained with sorbitol supplemented arabinose is not significantly different to flies trained with sucrose (p>0.6). Asterisks denote significant difference between marked groups and others (p< 0.05, arabinose; p<0.01 sorbitol, ANOVA). Data are mean ± SEM. n≥14. (D) Training with sorbitol supplemented xylose forms persistent memory. 24hr appetitive memory performance of flies trained with sorbitol supplemented xylose is not significantly different to flies trained with sucrose (p>0.6). Asterisks denote significant difference between marked groups and others (p <0.05, xylose; p<0.01 sorbitol, ANOVA). Data are mean ± SEM. n≥14. (E) More dyed sorbitol is consumed in 5min when mixed with arabinose or xylose. Each substance or combination was mixed with dye and presented dried on filter paper in the conditioning apparatus. The amount ingested with arabinose+sorbitol or xylose+sorbitol was statistically different to sorbitol (p<0.05 and p<0.01 respectively) or water alone (both p<0.01, ANOVA). Consumption of dye with sorbitol was not statistically different from dye with water (p>0.05). Data are mean ± SEM. n≥8.
Figure 3
Figure 3. Nutrient information is rapidly coded and can be used to guide preference behavior immediately after training
Flies were differentially conditioned by pairing one odor with one sugar and the other odor with a different sugar, or supplemented sugar. They were then immediately tested for olfactory preference. Flies always exhibited preference for the odor that had been previously paired with a substance with nutrient value – sucrose over arabinose; arabinose+sorbitol over arabinose alone. They showed no preference when both odors were paired with nutritious substance – sucrose versus fructose; sucrose versus arabinose+sorbitol. Both of these scores were not statistically different from zero (both p>0.6, Mann Whitney U test). Data are mean ± SEM. n≥10.

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