Sleep regulates visual selective attention in Drosophila

Abstract

Although sleep deprivation is known to impair attention in humans and other mammals, the underlying reasons are not well understood, and whether similar effects are present in non-mammalian species is not known. We therefore sought to investigate whether sleep is important for optimizing attention in an invertebrate species, the genetic model Drosophila melanogaster. We developed a highthroughput paradigm to measure visual attention in freely walking Drosophila, using competing foreground/background visual stimuli. We found that whereas sleep-deprived flies could respond normally to either stimulus alone, they were more distracted by background cues in a visual competition task. Other stressful manipulations such as starvation, heat exposure and mechanical stress had no effects on visual attention in this paradigm. In contrast to sleep deprivation, providing additional sleep using the GABA-A agonist 4,5,6,7tetrahydroisoxazolo-[5,4-c]pyridine-3-ol (THIP) did not affect attention in wild-type flies, but specifically improved attention in the learning mutant dunce. Our results reveal a key function of sleep in optimizing attention processes in Drosophila, and establish a behavioral paradigm that can be used to explore the molecular mechanisms involved.

Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila

“…1A). Previous studies implicated the CX in the higher control of behavior, including locomotion, orientation and courtship behavior, visual memory and place learning as well as attention, arousal and decision-making [24][25][26][27][28][29][30][31][32][33][34][35][36][37] . Although triggered by different sensory modalities, the gating of these behaviors involves two major types of projection neurons that characterize the circuit architecture of the CX (Fig.…”

Visual experience drives sleep need in Drosophila

“…To better understand the visual defects of omb flies, we next performed a thorough characterization of visual behavior in omb and wild-type flies in a recently developed arena for freely walking flies [4, 32], based on Buridan’s paradigm [32]. In our visual arena, we examined optomotor responses (tendency to turn in the same direction as a moving grating), and fixation behavior (orientation and walking back and forth between two objects), and looked at changes in visual responses of wild-type and omb mutants as we altered grating speed and object flicker frequency (Figure 2, B and C).…”

“…We used a modified version of Buridan’s paradigm [32] as described previously [4, 33]. Briefly flies with clipped wings walked freely on a platform surrounded by a water-filled moat (preventing escape).…”

“…Visual behavior was analyzed with CeTran (3.4) software [34], and with custom-made scripts in R programming language, as previously [4, 33]. Briefly stripe deviation was calculated as the smallest angle between the fly’s trajectory and either of the vertical objects [34], whereas optomotor responses represented the angular velocity of the fly (turning angle/second) moving in the grating direction.…”

“…The reasons for variation in sleep need are unclear, but may relate to distinct sleep functions that are homeostatically regulated. Sleep is crucial for learning, attention, and memory formation [2, 3], and these processes appear to be conserved among animals, as sleep maintains attention processes even in the fruit fly, Drosophila melanogaster [4]. Sleep is a homeostatic process, which adjusts to experiences during wakefulness by driving plasticity processes during sleep [5–8].…”