TY - JOUR
T1 - Sleep deprivation, sleep fragmentation, and social jet lag increase temperature preference in Drosophila
AU - Roach, S. Tanner
AU - Ford, Melanie C.
AU - Simhambhatla, Vikram
AU - Loutrianakis, Vasilios
AU - Farah, Hamza
AU - Li, Zhaoyi
AU - Periandri, Erica M.
AU - Abdalla, Dina
AU - Huang, Irene
AU - Kalra, Arjan
AU - Shaw, Paul J.
N1 - Publisher Copyright:
Copyright © 2023 Roach, Ford, Simhambhatla, Loutrianakis, Farah, Li, Periandri, Abdalla, Huang, Kalra and Shaw.
PY - 2023
Y1 - 2023
N2 - Despite the fact that sleep deprivation substantially affects the way animals regulate their body temperature, the specific mechanisms behind this phenomenon are not well understood. In both mammals and flies, neural circuits regulating sleep and thermoregulation overlap, suggesting an interdependence that may be relevant for sleep function. To investigate this relationship further, we exposed flies to 12 h of sleep deprivation, or 48 h of sleep fragmentation and evaluated temperature preference in a thermal gradient. Flies exposed to 12 h of sleep deprivation chose warmer temperatures after sleep deprivation. Importantly, sleep fragmentation, which prevents flies from entering deeper stages of sleep, but does not activate sleep homeostatic mechanisms nor induce impairments in short-term memory also resulted in flies choosing warmer temperatures. To identify the underlying neuronal circuits, we used RNAi to knock down the receptor for Pigment dispersing factor, a peptide that influences circadian rhythms, temperature preference and sleep. Expressing UAS-PdfrRNAi in subsets of clock neurons prevented sleep fragmentation from increasing temperature preference. Finally, we evaluated temperature preference after flies had undergone a social jet lag protocol which is known to disrupt clock neurons. In this protocol, flies experience a 3 h light phase delay on Friday followed by a 3 h light advance on Sunday evening. Flies exposed to social jet lag exhibited an increase in temperature preference which persisted for several days. Our findings identify specific clock neurons that are modulated by sleep disruption to increase temperature preference. Moreover, our data indicate that temperature preference may be a more sensitive indicator of sleep disruption than learning and memory.
AB - Despite the fact that sleep deprivation substantially affects the way animals regulate their body temperature, the specific mechanisms behind this phenomenon are not well understood. In both mammals and flies, neural circuits regulating sleep and thermoregulation overlap, suggesting an interdependence that may be relevant for sleep function. To investigate this relationship further, we exposed flies to 12 h of sleep deprivation, or 48 h of sleep fragmentation and evaluated temperature preference in a thermal gradient. Flies exposed to 12 h of sleep deprivation chose warmer temperatures after sleep deprivation. Importantly, sleep fragmentation, which prevents flies from entering deeper stages of sleep, but does not activate sleep homeostatic mechanisms nor induce impairments in short-term memory also resulted in flies choosing warmer temperatures. To identify the underlying neuronal circuits, we used RNAi to knock down the receptor for Pigment dispersing factor, a peptide that influences circadian rhythms, temperature preference and sleep. Expressing UAS-PdfrRNAi in subsets of clock neurons prevented sleep fragmentation from increasing temperature preference. Finally, we evaluated temperature preference after flies had undergone a social jet lag protocol which is known to disrupt clock neurons. In this protocol, flies experience a 3 h light phase delay on Friday followed by a 3 h light advance on Sunday evening. Flies exposed to social jet lag exhibited an increase in temperature preference which persisted for several days. Our findings identify specific clock neurons that are modulated by sleep disruption to increase temperature preference. Moreover, our data indicate that temperature preference may be a more sensitive indicator of sleep disruption than learning and memory.
KW - Drosophila
KW - sleep
KW - sleep deprivation
KW - sleep fragmentation
KW - temperature preference behavior
UR - http://www.scopus.com/inward/record.url?scp=85161007832&partnerID=8YFLogxK
U2 - 10.3389/fnins.2023.1175478
DO - 10.3389/fnins.2023.1175478
M3 - Article
C2 - 37274220
AN - SCOPUS:85161007832
SN - 1662-4548
VL - 17
JO - Frontiers in Neuroscience
JF - Frontiers in Neuroscience
M1 - 1175478
ER -