Flies Remember the Time of Day

Abstract

The circadian clock enables organisms to anticipate daily environmental cycles and drives corresponding changes in behavior [1, 2]. Such endogenous oscillators also enable animals to display time-specific memory [1, 3-5]. For instance, mice and honeybees associate the location of a stimulus (like food or mate) with a certain time of day (time-place learning) [6, 7]. However, the mechanism underlying time-related learning and memory is not known. In the present study, we investigate time-specific odor learning. We use a genetically tractable animal, the fly Drosophila melanogaster. Starved flies are trained in the morning and afternoon to associate distinct odors with sucrose reward. The training is repeated the next day, and their time-dependent odor preference is tested on the third day. Our results indicate that Drosophila can express appetitive memory at the relevant time of day if the two conditioning events are separated by more than 4 hr. Flies can form time-odor associations in constant darkness (DD) as well as in a daily light-dark (LD) cycle, but not when kept under constant light (LL) conditions. Circadian clock mutants, period(01) (per(01)) and clock(AR) (clk(AR)), learned to associate sucrose reward with a certain odor but were unable to form time-odor associations. Our findings show that flies can utilize temporal information as an additional cue in appetitive learning. Time-odor learning in flies depends on a per- and clk-dependent endogenous mechanism that is independent of environmental light cues.

Regulation of olfactory associative memory by the circadian clock output signal Pigment-dispersing factor (PDF)

“…It's important 504 nevertheless to explore why, in the context of appetitive STM (which is ultimately TOD-505 independent), an organism's capacity for appetitive learning should be so critically linked to its 506 timekeeping capabilities. Though prior work is conflicting regarding TOD influence on 507 associative STM (Fropf et al, 2018;Lyons & Roman, 2009), TOD effects are consistently found 508 in associative LTM (Chouhan et al, 2015(Chouhan et al, , 2017Fropf et al, 2014Fropf et al, , 2018Lyons & Roman, 2009). 509…”

Heliconiini butterflies can learn time-dependent reward associations

“…However, our data on Dryas suggest that elaborated mushroom bodies are not necessary for the time learning abilities displayed in these taxa. This is further supported by the fact that Drosophila , which have substantially smaller mushroom bodies, can also learn time-dependent olfactory associations [14]. Therefore, the neural basis of integrating time information with foraging cues may be relatively simple.…”

“…For example, honey bees can consistently change their preference towards particular visual cues throughout the day [10,11], and some nectarivorous ants remember the time of day at which resources are most profitable [12,13]. However, the ability to learn time-dependent associations has only been formally demonstrated in a handful of invertebrates, including Drosophila , bees, and ants [11,14–21], and there is evidence that this ability can vary across species from the same family [12,13,22]. Hence, the prevalence of this ability, and the ecological factors that may account for its variability, are unclear.…”

FlyClockbase: Importance of Biological Model Curation for Analyzing Variability in the Circadian Clock of Drosophila melanogaster by Integrating Time Series from 25 Years of Research

“…2016), learning and memory (X u et al . 2008; C houhan et al . 2015), stress and immunity (D umbell et al .…”

“…Circadian clocks are biochemical pathways characterized by cyclical protein expression. They play a critical role in a wide variety of behavioral and physiological processes, and a better understanding of their genetic and biochemical bases could advance research in many areas (P reussner and H eyd 2016; S harma et al 2016), including consciousness and sleep (C irelli 2009), feeding and metabolism (X u et al 2008; H urley et al 2016), learning and memory (X u et al 2008; C houhan et al 2015), stress and immunity (D umbell et al 2016), inflammation (C arter et al 2016), cancer (S ephton and S piegel 2003; M asri et al 2015; S alavaty 2015; M olina -R odríguez and Á lvarez 2016), and psychological functioning (M c C lung 2013; P arekh et al 2015; C oogan et al 2016).…”