Use-Dependent Plasticity in Clock Neurons Regulates Sleep Need in Drosophila

Sleep is important for memory consolidation and is responsive to waking experience. Clock circuitry is uniquely positioned to coordinate interactions between processes underlying memory and sleep need. Flies increase sleep both after exposure to an enriched social environment and after protocols that induce long-term memory. We found that flies mutant for rutabaga, period, and blistered were deficient for experience-dependent increases in sleep. Rescue of each of these genes within the ventral lateral neurons (LNVs) restores increased sleep after social enrichment. Social experiences that induce increased sleep were associated with an increase in the number of synaptic terminals in the LNV projections into the medulla. The number of synaptic terminals was reduced during sleep and this decline was prevented by sleep deprivation.

[1]  Huifu Guo,et al.  PAR-1 Kinase Phosphorylates Dlg and Regulates Its Postsynaptic Targeting at the Drosophila Neuromuscular Junction , 2007, Neuron.

[2]  S. Eaton,et al.  Blistered: a gene required for vein/intervein formation in wings of Drosophila. , 1994, Development.

[3]  M. F. Ceriani,et al.  Circadian Remodeling of Neuronal Circuits Involved in Rhythmic Behavior , 2008, PLoS biology.

[4]  W. Gehring,et al.  The Drosophila SRF homolog is expressed in a subset of tracheal cells and maps within a genomic region required for tracheal development. , 1994, Development.

[5]  Alfred Nordheim,et al.  Serum response factor controls neuronal circuit assembly in the hippocampus , 2006, Nature Neuroscience.

[6]  A. Pack,et al.  Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. , 2003, Learning & memory.

[7]  A. Rechtschaffen,et al.  Physiological correlates of prolonged sleep deprivation in rats. , 1983, Science.

[8]  Ralph J Greenspan,et al.  Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila , 2007, Nature Neuroscience.

[9]  Paul J Shaw,et al.  Waking Experience Affects Sleep Need in Drosophila , 2006, Science.

[10]  M. Krasnow,et al.  The Drosophila Serum Response Factor gene is required for the formation of intervein tissue of the wing and is allelic to blistered. , 1996, Development.

[11]  K. J. Fogle,et al.  Large Ventral Lateral Neurons Modulate Arousal and Sleep in Drosophila , 2008, Current Biology.

[12]  J. Blanchard,et al.  Expression and purification of the DNA-binding domain of SRF: SRF-DB, a part of a DNA-binding protein which can act as a dominant negative mutant in vivo. , 1993, Experimental cell research.

[13]  G. Tononi,et al.  Sleep and synaptic homeostasis: a hypothesis , 2003, Brain Research Bulletin.

[14]  A. Garcı́a-Bellido,et al.  Genetic interactions and cell behaviour in blistered mutants during proliferation and differentiation of the Drosophila wing. , 1998, Development.

[15]  R. Stickgold,et al.  Practice with Sleep Makes Perfect Sleep-Dependent Motor Skill Learning , 2002, Neuron.

[16]  T. Kitamoto,et al.  A clock gene, period, plays a key role in long-term memory formation in Drosophila. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  T. Page,et al.  Circadian regulation of insect olfactory learning , 2007, Proceedings of the National Academy of Sciences.

[18]  Thomas Lemberger,et al.  SRF mediates activity-induced gene expression and synaptic plasticity but not neuronal viability , 2005, Nature Neuroscience.

[19]  Uwe Homberg,et al.  Pigment‐dispersing hormone‐immunoreactive neurons in the nervous system of wild‐type Drosophila melanogaster and of several mutants with altered circadian rhythmicity , 1993, The Journal of comparative neurology.

[20]  E. Kandel,et al.  A Role in Learning for SRF: Deletion in the Adult Forebrain Disrupts LTD and the Formation of an Immediate Memory of a Novel Context , 2006, Neuron.

[21]  M. Rosbash,et al.  Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain , 2008, Proceedings of the National Academy of Sciences.

[22]  M Heisenberg,et al.  Vision affects mushroom bodies and central complex in Drosophila melanogaster. , 1997, Learning & memory.

[23]  G. Tononi,et al.  Stress response genes protect against lethal effects of sleep deprivation in Drosophila , 2002, Nature.