Interaction of inhibitory and facilitatory effects of conditioning trials on long-term memory formation

Animals learn through experience and consolidate the memories into long-time storage. Conditioning parameters to induce protein synthesis-dependent long-term memory (LTM) have been the subject of extensive studies in many animals. Here we found a case in which a conditioning trial inhibits or facilitates LTM formation depending on the intervals from preceding trials. We studied the effects of conditioning parameters on LTM formation in olfactory conditioning of maxillary-palpi extension response with sucrose reward in the cockroach Periplaneta americana We found, at first, that translation- and transcription-dependent LTM forms 1 h after training, the fastest so far reported in insects. Second, we observed that multiple-trial training with an intertrial interval (ITI) of 20 or 30 sec, often called massed training, is more effective than spaced training for LTM formation, an observation that differs from the results of most studies in other animals. Third, we found that a conditioning trial inhibits LTM formation when the intervals from preceding trials were in the range of 10-16 min. This inhibitory effect is pairing-specific and is not due to decreased motivation for learning (overtraining effect). To our knowledge, no similar inhibition of LTM formation by a conditioning trial has been reported in any animals. We propose a model to account for the effects of trial number and ITIs on LTM formation. Olfactory conditioning in cockroaches should provide pertinent materials in which to study neuronal and molecular mechanisms underlying the inhibitory and facilitatory processes for LTM formation.

[1]  M. Mizunami,et al.  Salivary conditioning with antennal gustatory unconditioned stimulus in an insect , 2008, Neurobiology of Learning and Memory.

[2]  L. Kamin,et al.  The retention of an incompletely learned avoidance response. , 1957, Journal of comparative and physiological psychology.

[3]  H. Pashler,et al.  Distributed practice in verbal recall tasks: A review and quantitative synthesis. , 2006, Psychological bulletin.

[4]  Michael A Sutton,et al.  Interaction between amount and pattern of training in the induction of intermediate- and long-term memory for sensitization in aplysia. , 2002, Learning & memory.

[5]  Yadin Dudai,et al.  Memorable Trends , 2013, Neuron.

[6]  S. Klein,et al.  Forgetting by the rat after intermediate intervals ("Kamin effect") as retrieval failure. , 1970 .

[7]  M. Mizunami,et al.  Participation of NO signaling in formation of long-term memory in salivary conditioning of the cockroach , 2013, Neuroscience Letters.

[8]  M. Mizunami,et al.  Olfactory Learning and Memory in the Cockroach Periplaneta americana , 2001 .

[9]  T. Carew,et al.  Transient Mitogen-Activated Protein Kinase Activation Is Confined to a Narrow Temporal Window Required for the Induction of Two-Trial Long-Term Memory in Aplysia , 2007, The Journal of Neuroscience.

[10]  R. Menzel,et al.  Contextual modulation of memory consolidation. , 2000, Learning & memory.

[11]  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.

[12]  M. Bouton,et al.  Analysis of a trial-spacing effect with relatively long intertrial intervals , 2008, Learning & behavior.

[13]  G. D. SANDERS,et al.  Variations in Retention Performance during Long Term Memory Formation , 1971, Nature.

[14]  Paul R. Benjamin,et al.  Susceptibility of memory consolidation during lapses in recall , 2013, Nature Communications.

[15]  M. Mizunami,et al.  Classical Olfactory Conditioning in the Cockroach Periplaneta americana , 2003, Zoological science.

[16]  M. Mizunami,et al.  Temporal determinants of long-term retention of olfactory memory in the cricket Gryllus bimaculatus. , 2002, The Journal of experimental biology.

[17]  M. Mizunami,et al.  Time Course of Protein Synthesis-Dependent Phase of Olfactory Memory in the Cricket Gryllus bimaculatus , 2003, Zoological science.

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

[19]  Randolf Menzel,et al.  Behavioural access to short-term memory in bees , 1979, Nature.

[20]  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.

[21]  W. Sossin,et al.  Molecular Determinants of the Spacing Effect , 2012, Neural plasticity.

[22]  M. Mizunami,et al.  Pheromone detection by a pheromone emitter: a small sex pheromone-specific processing system in the female American cockroach. , 2011, Chemical senses.

[23]  Edward L. Bennett,et al.  Short-term, intermediate-term, and long-term memories , 1993, Behavioural Brain Research.

[24]  M. Mizunami,et al.  Roles of octopamine and dopamine in appetitive and aversive memory acquisition studied in olfactory conditioning of maxillary palpi extension response in crickets , 2015, Front. Behav. Neurosci..

[25]  Paul Smolen,et al.  Computational Design of Enhanced Learning Protocols , 2011, Nature Neuroscience.

[26]  Coarse topographic organization of pheromone-sensitive afferents from different antennal surfaces in the American cockroach , 2015, Neuroscience Letters.

[27]  M. Mizunami,et al.  Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee , 2014, Learning & memory.

[28]  J. Boeckh,et al.  Contribution of single unit analysis in insects to an understanding of olfactory function , 1987, Journal of Comparative Physiology A.

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

[30]  Bruce D. Gelb,et al.  The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction , 2009, Cell.

[31]  M. Mizunami,et al.  Classical conditioning of activities of salivary neurones in the cockroach , 2006, Journal of Experimental Biology.

[32]  M. Mizunami,et al.  Complete mapping of glomeruli based on sensory nerve branching pattern in the primary olfactory center of the cockroach Periplaneta americana , 2010, The Journal of comparative neurology.

[33]  Makoto Mizunami,et al.  Pavlov's Cockroach: Classical Conditioning of Salivation in an Insect , 2007, PloS one.

[34]  M. Mizunami,et al.  Roles of OA1 octopamine receptor and Dop1 dopamine receptor in mediating appetitive and aversive reinforcement revealed by RNAi studies , 2016, Scientific Reports.

[35]  R. Menzel Memory dynamics in the honeybee , 1999, Journal of Comparative Physiology A.

[36]  Ronald L. Davis,et al.  A Late-Phase, Long-Term Memory Trace Forms in the γ Neurons of Drosophila Mushroom Bodies after Olfactory Classical Conditioning , 2010, The Journal of Neuroscience.

[37]  Y. Dudai The restless engram: consolidations never end. , 2012, Annual review of neuroscience.

[38]  Yukihisa Matsumoto,et al.  Contextual olfactory learning in cockroaches , 2006, Neuroreport.

[39]  M. Mizunami,et al.  Olfactory discrimination of structurally similar alcohols by cockroaches , 2002, Journal of Comparative Physiology A.

[40]  M. Mizunami,et al.  Critical roles of mecamylamine-sensitive mushroom body neurons in insect olfactory learning , 2011, Neurobiology of Learning and Memory.

[41]  W. Riege,et al.  One-Trial Learning and Biphasic Time Course of Performance in the Goldfish , 1971, Science.

[42]  M. Hammer,et al.  Backward inhibitory learning in honeybees: a behavioral analysis of reinforcement processing. , 1998, Learning & memory.

[43]  M. Mizunami,et al.  Context-dependent olfactory learning monitored by activities of salivary neurons in cockroaches , 2012, Neurobiology of Learning and Memory.

[44]  M. Papini,et al.  Massed Trial Overtraining Effects on Extinction and Reversal Performance in Turtles (Geoclemys Reevesii) , 1997 .

[45]  M. Mizunami,et al.  Visual and olfactory input segregation in the mushroom body calyces in a basal neopteran, the American cockroach. , 2012, Arthropod structure & development.

[46]  J. Dubnau,et al.  Deconstructing Memory in Drosophila , 2005, Current Biology.

[47]  E. Kandel,et al.  The Molecular and Systems Biology of Memory , 2014, Cell.

[48]  S. Rose,et al.  Two critical periods of protein and glycoprotein synthesis in memory consolidation for visual categorization learning in chicks. , 1998, Learning & memory.

[49]  G. G. Ball,et al.  Reversal and transfer learning following overtraining in rat and chicken. , 1961 .

[50]  M. Mizunami,et al.  Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory. , 2006, Learning & memory.