Neuronal reactivation during post-learning sleep consolidates long-term memory in Drosophila

Animals consolidate some, but not all, learning experiences into long-term memory. Across the animal kingdom, sleep has been found to have a beneficial effect on the consolidation of recently formed memories into long-term storage. However, the underlying mechanisms of sleep dependent memory consolidation are poorly understood. Here, we show that consolidation of courtship long-term memory in Drosophila is mediated by reactivation during sleep of dopaminergic neurons that were earlier involved in memory acquisition. We identify specific fan-shaped body neurons that induce sleep after the learning experience and activate dopaminergic neurons for memory consolidation. Thus, we provide a direct link between sleep, neuronal reactivation of dopaminergic neurons, and memory consolidation.

[1]  Giulio Tononi,et al.  Sleep and Synaptic Homeostasis: Structural Evidence in Drosophila , 2011, Science.

[2]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[3]  A. Kral,et al.  Erratum to “Development of Brainstem-Evoked Responses in Congenital Auditory Deprivation” , 2012, Neural Plasticity.

[4]  R. Stickgold,et al.  Sleep, memory, and plasticity. , 2006, Annual review of psychology.

[5]  Gerald M. Rubin,et al.  Control of Sleep by Dopaminergic Inputs to the Drosophila Mushroom Body , 2015, Front. Neural Circuits.

[6]  J. Galvin,et al.  Persistent short-term memory defects following sleep deprivation in a drosophila model of Parkinson disease. , 2009, Sleep.

[7]  Gerald M. Rubin,et al.  Propagation of Homeostatic Sleep Signals by Segregated Synaptic Microcircuits of the Drosophila Mushroom Body , 2015, Current Biology.

[8]  C. Smith.  Sleep states and memory processes in humans: procedural versus declarative memory systems. , 2001, Sleep medicine reviews.

[9]  J. Born,et al.  The contribution of sleep to hippocampus-dependent memory consolidation , 2007, Trends in Cognitive Sciences.

[10]  M. Rosbash,et al.  Genome-wide identification of neuronal activity-regulated genes in Drosophila , 2016, eLife.

[11]  Barry J Dickson,et al.  Persistent activity in a recurrent circuit underlies courtship memory in Drosophila , 2018, eLife.

[12]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[13]  G. Rubin,et al.  The neuronal architecture of the mushroom body provides a logic for associative learning , 2014, eLife.

[14]  G. Rubin,et al.  Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila , 2014, eLife.

[15]  A. Grosmark,et al.  Dopaminergic Control of Sleep–Wake States , 2006, The Journal of Neuroscience.

[16]  Qili Liu,et al.  Sleep Drive Is Encoded by Neural Plastic Changes in a Dedicated Circuit , 2016, Cell.

[17]  G. Tononi,et al.  Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration , 2014, Neuron.

[18]  A Borst,et al.  Drosophila mushroom body mutants are deficient in olfactory learning. , 1985, Journal of neurogenetics.

[19]  K. Iliadi,et al.  Drosophila conditioned courtship: two ways of testing memory. , 1999, Learning & memory.

[20]  M. Wilson,et al.  VTA neurons coordinate with the hippocampal reactivation of spatial experience , 2015, eLife.

[21]  G. Rubin,et al.  Tools for neuroanatomy and neurogenetics in Drosophila , 2008, Proceedings of the National Academy of Sciences.

[22]  D. Dinges,et al.  Neurocognitive consequences of sleep deprivation. , 2005, Seminars in neurology.

[23]  A. Patapoutian,et al.  Ion channels: Opposite thermosensor in fruitfly and mouse , 2003, Nature.

[24]  M. Rosbash,et al.  Temporal calcium profiling of specific circadian neurons in freely moving flies , 2017, Proceedings of the National Academy of Sciences.

[25]  B. Mensh,et al.  Synaptic Orb2A Bridges Memory Acquisition and Late Memory Consolidation in Drosophila , 2015, Cell reports.

[26]  Wolfram Schultz,et al.  Multiple functions of dopamine neurons , 2010, F1000 biology reports.

[27]  B. Swinderen,et al.  The Yin and Yang of Sleep and Attention , 2015, Trends in Neurosciences.

[28]  G. Tononi,et al.  Correlates of sleep and waking in Drosophila melanogaster. , 2000, Science.

[29]  Gero Miesenböck,et al.  Neuronal Machinery of Sleep Homeostasis in Drosophila , 2014, Neuron.

[30]  Julie H. Simpson,et al.  A GAL4-driver line resource for Drosophila neurobiology. , 2012, Cell reports.

[31]  Jai Y. Yu,et al.  Dopamine neurons modulate pheromone responses in Drosophila courtship learning , 2012, Nature.

[32]  P. Shaw,et al.  Sleep, Performance, and Memory in Flies , 2015, Current Sleep Medicine Reports.

[33]  B. van Swinderen,et al.  A Dynamic Deep Sleep Stage in Drosophila , 2013, The Journal of Neuroscience.

[34]  P. Wong,et al.  Paradoxical sleep increases predict successful learning in a complex operant task. , 1991, Behavioral neuroscience.

[35]  G. Rubin,et al.  Refinement of Tools for Targeted Gene Expression in Drosophila , 2010, Genetics.

[36]  E. Kandel.  The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses , 2001, Science.

[37]  I. Izquierdo,et al.  Dopamine Controls Persistence of Long-Term Memory Storage , 2009, Science.

[38]  Aljoscha Nern,et al.  Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system , 2015, Proceedings of the National Academy of Sciences.

[39]  Yadin Dudai,et al.  The Consolidation and Transformation of Memory , 2015, Neuron.

[40]  T. Kitamoto.  TARGETED EXPRESSION OF TEMPERATURE-SENSITIVE DYNAMIN TO STUDY NEURAL MECHANISMS OF COMPLEX BEHAVIOR IN Drosophila , 2002, Journal of neurogenetics.

[41]  B. Swinderen,et al.  Sleep Restores Behavioral Plasticity to Drosophila Mutants , 2015, Current Biology.

[42]  M. Frank,et al.  Erasing Synapses in Sleep: Is It Time to Be SHY? , 2012, Neural plasticity.

[43]  P. Garrity,et al.  The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. , 2005, Genes & development.

[44]  Allan I Pack,et al.  Rest in Drosophila Is a Sleep-like State , 2000, Neuron.

[45]  J. Born,et al.  The memory function of sleep , 2010, Nature Reviews Neuroscience.

[46]  E. Z. Kim,et al.  High-Resolution Positional Tracking for Long-Term Analysis of Drosophila Sleep and Locomotion Using the “Tracker” Program , 2012, PloS one.

[47]  Matthew S. Thimgan,et al.  Inducing Sleep by Remote Control Facilitates Memory Consolidation in Drosophila , 2011, Science.

[48]  J. Levine,et al.  Sequential Learning of Pheromonal Cues Modulates Memory Consolidation in Trainer-Specific Associative Courtship Conditioning , 2005, Current Biology.

[49]  G. Miesenböck,et al.  Operation of a Homeostatic Sleep Switch , 2016, Nature.

[50]  K. Siwicki,et al.  Associative learning and memory in Drosophila: beyond olfactory conditioning , 2003, Behavioural Processes.

[51]  F. Conti,et al.  Tonic and phasic tetrodotoxin block of sodium channels with point mutations in the outer pore region. , 1999, Biophysical journal.

[52]  Daniel J. R. Christensen,et al.  Sleep Drives Metabolite Clearance from the Adult Brain , 2013, Science.

[53]  Angelique C. Paulk,et al.  Oscillatory brain activity in spontaneous and induced sleep stages in flies , 2017, Nature Communications.

[54]  Michael B. Reiser,et al.  Behavioral state modulates the ON visual motion pathway of Drosophila , 2017, Proceedings of the National Academy of Sciences.

[55]  Barry J. Dickson,et al.  The VT GAL4, LexA, and split-GAL4 driver line collections for targeted expression in the Drosophila nervous system , 2017, bioRxiv.

[56]  J. Born,et al.  Neuroscience and Biobehavioral Reviews Sleep and Memory in Mammals, Birds and Invertebrates , 2022 .

[57]  Haojiang Luan,et al.  Refined Spatial Manipulation of Neuronal Function by Combinatorial Restriction of Transgene Expression , 2006, Neuron.

[58]  J. Born,et al.  Learning-Dependent Increases in Sleep Spindle Density , 2002, The Journal of Neuroscience.

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

[60]  P. Shaw,et al.  D1 Receptor Activation in the Mushroom Bodies Rescues Sleep-Loss-Induced Learning Impairments in Drosophila , 2008, Current Biology.

[61]  Stefan R. Pulver,et al.  Independent Optical Excitation of Distinct Neural Populations , 2014, Nature Methods.