A role of protein degradation in memory consolidation after initial learning and extinction learning in the honeybee (Apis mellifera).

Protein degradation is known to affect memory formation after extinction learning. We demonstrate here that an inhibitor of protein degradation, MG132, interferes with memory formation after extinction learning in a classical appetitive conditioning paradigm. In addition, we find an enhancement of memory formation when the same inhibitor is applied after initial learning. This result supports the idea that MG132 targets an ongoing consolidation process. Furthermore, we demonstrate that the sensitivity of memory formation after initial learning and extinction learning to MG132 depends in the same way on the number of CS-US trials and the intertrial interval applied during initial learning. This supports the idea that the learning parameters during acquisition are critical for memory formation after extinction and that protein degradation in both learning processes might be functionally linked.

[1]  K. Lattal,et al.  9YExtinction: Does It or Doesn’t It? The Requirement of Altered Gene Activity and New Protein Synthesis , 2006, Biological Psychiatry.

[2]  P. Masson,et al.  Identification and Characterization of a Drosophila Proteasome Regulatory Network , 2005, Molecular and Cellular Biology.

[3]  M. Bitterman,et al.  Classical conditioning of proboscis extension in honeybees (Apis mellifera). , 1983, Journal of comparative psychology.

[4]  T. Préat,et al.  Genetic dissection of consolidated memory in Drosophila , 1994, Cell.

[5]  M. Bouton Context and behavioral processes in extinction. , 2004, Learning & memory.

[6]  A. Goldberg,et al.  Proteasome inhibitors: from research tools to drug candidates. , 2001, Chemistry & biology.

[7]  S. Kunes,et al.  Synaptic Protein Synthesis Associated with Memory Is Regulated by the RISC Pathway in Drosophila , 2006, Cell.

[8]  Sue-Hyun Lee,et al.  Synaptic Protein Degradation Underlies Destabilization of Retrieved Fear Memory , 2008, Science.

[9]  Randolf Menzel,et al.  Spontaneous Recovery from Extinction Depends on the Reconsolidation of the Acquisition Memory in an Appetitive Learning Paradigm in the Honeybee (Apis mellifera) , 2005, The Journal of Neuroscience.

[10]  Richard Paylor,et al.  Dynamic Translational and Proteasomal Regulation of Fragile X Mental Retardation Protein Controls mGluR-Dependent Long-Term Depression , 2006, Neuron.

[11]  S. Matsumoto,et al.  Formation of Bombyx mori nucleopolyhedrovirus IE2 nuclear foci is regulated by the functional domains for oligomerization and ubiquitin ligase activity. , 2005, The Journal of general virology.

[12]  G. H. Lunney,et al.  USING ANALYSIS OF VARIANCE WITH A DICHOTOMOUS DEPENDENT VARIABLE: AN EMPIRICAL STUDY , 1970 .

[13]  R. Menzel,et al.  Temporal Determinants of Olfactory Long-Term Retention in Honeybee Classical Conditioning: Nonmonotonous Effects of the Training Trial Interval , 1998, Neurobiology of Learning and Memory.

[14]  U. Müller,et al.  Learning at Different Satiation Levels Reveals Parallel Functions for the cAMP–Protein Kinase A Cascade in Formation of Long-Term Memory , 2004, The Journal of Neuroscience.

[15]  I. Izquierdo,et al.  The ubiquitin–proteasome cascade is required for mammalian long‐term memory formation , 2001, The European journal of neuroscience.

[16]  K. Kosik,et al.  A Coordinated Local Translational Control Point at the Synapse Involving Relief from Silencing and MOV10 Degradation , 2009, Neuron.

[17]  K. Martin,et al.  The Ubiquitin Proteasome System Functions as an Inhibitory Constraint on Synaptic Strengthening , 2003, Current Biology.

[18]  P. Roullet,et al.  Protein degradation, as with protein synthesis, is required during not only long‐term spatial memory consolidation but also reconsolidation , 2008, The European journal of neuroscience.

[19]  E. Merlo,et al.  Long-term memory consolidation depends on proteasome activity in the crab Chasmagnathus , 2007, Neuroscience.

[20]  Michael Davis,et al.  Behavioral and Neural Analysis of Extinction , 2002, Neuron.

[21]  Y. Dudai The neurobiology of consolidations, or, how stable is the engram? , 2004, Annual review of psychology.

[22]  I. Balderas,et al.  Long-term aversive taste memory requires insular and amygdala protein degradation , 2011, Neurobiology of Learning and Memory.

[23]  T. Shimada,et al.  Role of the ubiquitin-proteasome system in Bombyx mori nucleopolyhedrovirus infection. , 2011, The Journal of general virology.

[24]  P. Gean,et al.  Synaptic Expression of Glutamate Receptor after Encoding of Fear Memory in the Rat Amygdala , 2006, Molecular Pharmacology.

[25]  O. Hardt,et al.  A single standard for memory: the case for reconsolidation , 2009, Nature Reviews Neuroscience.

[26]  Timothy J Jarome,et al.  Activity Dependent Protein Degradation Is Critical for the Formation and Stability of Fear Memory in the Amygdala , 2011, PloS one.

[27]  Johannes Felsenberg,et al.  Behavioural Pharmacology in Classical Conditioning of the Proboscis Extension Response in Honeybees (Apis mellifera) , 2011, Journal of visualized experiments : JoVE.

[28]  A. Sehgal,et al.  A role for the proteasome in the light response of the timeless clock protein. , 1999, Science.

[29]  T. Bonhoeffer,et al.  A Balance of Protein Synthesis and Proteasome-Dependent Degradation Determines the Maintenance of LTP , 2006, Neuron.

[30]  Thuy K. Smith,et al.  Proteasome inhibition enhances the induction and impairs the maintenance of late-phase long-term potentiation. , 2008, Learning & memory.

[31]  M. Giurfa,et al.  Olfactory conditioning of the sting extension reflex in honeybees: Memory dependence on trial number, interstimulus interval, intertrial interval, and protein synthesis. , 2009, Learning & memory.

[32]  U. Müller,et al.  Induction of a Specific Olfactory Memory Leads to a Long-Lasting Activation of Protein Kinase C in the Antennal Lobe of the Honeybee , 1998, The Journal of Neuroscience.

[33]  Samuel Schacher,et al.  Mechanisms for Generating the Autonomous cAMP-Dependent Protein Kinase Required for Long-Term Facilitation in Aplysia , 1999, Neuron.

[34]  T. Knöpfel,et al.  Involvement of Protein Synthesis and Degradation in Long-Term Potentiation of Schaffer Collateral CA1 Synapses , 2006, The Journal of Neuroscience.

[35]  Thomas Preat,et al.  Exclusive Consolidated Memory Phases in Drosophila , 2004, Science.

[36]  M. Giurfa,et al.  Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees. , 2012, Learning & memory.

[37]  E. Skoulakis,et al.  Neuralized is expressed in the α/β lobes of adult Drosophila mushroom bodies and facilitates olfactory long-term memory formation , 2008, Proceedings of the National Academy of Sciences.

[38]  E. Lai,et al.  Xenopus neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling. , 2001, Developmental cell.

[39]  N. Stollhoff,et al.  Consolidation of an Extinction Memory Depends on the Unconditioned Stimulus Magnitude Previously Experienced during Training , 2009, The Journal of Neuroscience.

[40]  R. Menzel,et al.  Massed and spaced learning in honeybees: the role of CS, US, the intertrial interval, and the test interval. , 2001, Learning & memory.

[41]  R. Menzel,et al.  Long‐ but not medium‐term retention of olfactory memories in honeybees is impaired by actinomycin D and anisomycin , 1998, The European journal of neuroscience.

[42]  A. Lampin-Saint-Amaux,et al.  Debra, a Protein Mediating Lysosomal Degradation, Is Required for Long-Term Memory in Drosophila , 2011, PloS one.