Learning Performance of Normal and MutantDrosophila after Repeated Conditioning Trials with Discrete Stimuli

A new olfactory conditioning procedure is described using short training trials with discrete presentation of conditioned stimuli (CS) and unconditioned stimuli (US). A short odor presentation along with a single-shock stimulus produced modest but reliable and reproducible learning. Multiple trials presented sequentially improved performance with increasing trial number. Trial spacing had a significant impact on performance. Two trials presented with a short intertrial interval (ITI) produced no improvement over a single trial; two trials with a 15 min ITI significantly boosted performance. This effect required two associative trials, because substituting one of the trials with the CS alone, US alone, or an unpaired CS–US failed to boost performance. The increase in initial performance with two trials decayed within 15 min after training. Thus, the effect is short-lived. The utility of using a battery of tests, including a single short trial, two massed trials, and two spaced trials, to investigate parameters of memory formation in several mutants was demonstrated.

[1]  E R Kandel,et al.  A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. , 1986, Science.

[2]  T. Carew,et al.  Molecular Enhancement of Memory Formation , 1996, Neuron.

[3]  R. R. Miller,et al.  Trial spacing and trial distribution effects in Pavlovian conditioning: contributions of a comparator mechanism. , 1994, Journal of experimental psychology. Animal behavior processes.

[4]  Interactive contributions of intracellular calcium and protein phosphatases to massed-trials learning deficits in Hermissenda. , 1999, Behavioral neuroscience.

[5]  E. Miller,et al.  The Prefrontal Cortex Complex Neural Properties for Complex Behavior , 1999, Neuron.

[6]  T. Préat,et al.  Decreased Odor Avoidance after Electric Shock inDrosophila Mutants Biases Learning and Memory Tests , 1998, The Journal of Neuroscience.

[7]  Ronald L. Davis,et al.  Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster , 1981, Nature.

[8]  Ralph J. Greenspan,et al.  Inhibition of calcium/calmodulin-dependent protein kinase in drosophila disrupts behavioral plasticity , 1993, Neuron.

[9]  R. Rescorla Behavioral studies of Pavlovian conditioning. , 1988, Annual review of neuroscience.

[10]  M Heisenberg,et al.  Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. , 1994, Science.

[11]  R. Clark,et al.  Classical conditioning and brain systems: the role of awareness. , 1998, Science.

[12]  Eric R. Kandel,et al.  Long-Term Habituation of a Defensive Withdrawal Reflex in Aplysia , 1972, Science.

[13]  Ronald L. Davis,et al.  Olfactory Learning Deficits in Mutants for leonardo, a Drosophila Gene Encoding a 14-3-3 Protein , 1996, Neuron.

[14]  R. Lubow Latent inhibition as a measure of learned inattention: some problems and solutions , 1997, Behavioural Brain Research.

[15]  I. Weiner Neural substrates of latent inhibition: the switching model. , 1990, Psychological bulletin.

[16]  M. Livingstone,et al.  Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant , 1984, Cell.

[17]  Ronald L. Davis,et al.  Preferential expression of the drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects , 1992, Neuron.

[18]  Ronald L. Davis Mushroom bodies and drosophila learning , 1993, Neuron.

[19]  L. Thurstone Rank order as a psycho-physical method. , 1931 .

[20]  D. Scott Perceptual learning. , 1974, Queen's nursing journal.

[21]  Ronald L. Davis,et al.  The cyclic AMP phosphodiesterase encoded by the drosophila dunce gene is concentrated in the mushroom body neuropil , 1991, Neuron.

[22]  Ronald L. Davis,et al.  Integrin-mediated short-term memory in Drosophila , 1998, Nature.

[23]  R. Davis,et al.  Physiology and biochemistry of Drosophila learning mutants. , 1996, Physiological reviews.

[24]  Y. Jan,et al.  dunce, a mutant of Drosophila deficient in learning. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Alcino J. Silva,et al.  Spaced training induces normal long-term memory in CREB mutant mice , 1997, Current Biology.

[26]  M. Fanselow,et al.  Contextual conditioning with massed versus distributed unconditional stimuli in the absence of explicit conditional stimuli. , 1988, Journal of experimental psychology. Animal behavior processes.

[27]  Eric R. Kandel,et al.  Long-Term Sensitization of a Defensive Withdrawal Reflex in Aplysia , 1973, Science.

[28]  M Heisenberg,et al.  Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. , 1998, Learning & memory.

[29]  Ronald L. Davis,et al.  Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory , 1993, Neuron.

[30]  E. Kandel,et al.  Synapse-Specific, Long-Term Facilitation of Aplysia Sensory to Motor Synapses: A Function for Local Protein Synthesis in Memory Storage , 1997, Cell.

[31]  H. Maldonado,et al.  Context Shift and Protein Synthesis Inhibition Disrupt Long-Term Habituation after Spaced, but Not Massed, Training in the CrabChasmagnathus , 1999, Neurobiology of Learning and Memory.

[32]  Ronald L. Davis,et al.  The Drosophila learning and memory gene rutabaga encodes a Ca 2+ calmodulin -responsive , 1992, Cell.

[33]  D. Balota,et al.  Characteristics of associative learning in younger and older adults: evidence from an episodic priming paradigm. , 1996, Psychology and aging.

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