A novel intermediate stage in the transition between short- and long-term facilitation in the sensory to motor neuron synapse of aplysia

A major difference between short- and long-term memory is that long-term memory is dependent on new protein synthesis. Long-term memory can be further subdivided into a transient, initial phase that is readily susceptible to disruption and a later, more stable and persistent stage. To analyze this transition on the cellular level, we have examined the steps whereby short-term facilitation is converted to a long-term form in the sensorimotor connection of the Aplysia gill-withdrawal reflex. We found that stable long-term facilitation (at 24 hr) requires a higher concentration (100 nM) of serotonin (5-HT) than does short-term facilitation (10 nM). By using low concentrations of 5-HT, which do not produce long-term facilitation, we now have been able to explore the intermediate phases between the short- and long-term processes. By this means we have uncovered a new transient phase that involves three mechanistically different mechanisms--covalent modification, translation, and transcription--each of which can be recruited as a function of the concentration of 5-HT.

[1]  C. P. Duncan,et al.  The retroactive effect of electroshock on learning. , 1949, Journal of comparative and physiological psychology.

[2]  E. Kandel,et al.  Activation of cAMP-Responsive genes by stimuli that produce long-term facilitation in aplysia sensory neurons , 1993, Neuron.

[3]  W. Russell,et al.  The traumatic amnesias. , 1968, International journal of neurology.

[4]  E. Kandel,et al.  Long-term heterosynaptic inhibition in Aplysia , 1988, Nature.

[5]  N J Emptage,et al.  Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. , 1993, Science.

[6]  E. Kandel,et al.  Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. , 1990, Science.

[7]  E R Kandel,et al.  Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  E. Kandel,et al.  C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia , 1994, Cell.

[9]  E R Kandel,et al.  Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. , 1993, Science.

[10]  W N Frost,et al.  Monosynaptic connections made by the sensory neurons of the gill- and siphon-withdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[11]  E. Kandel,et al.  Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in aplysia sensory neurons , 1992, Neuron.

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

[13]  R. Hawkins,et al.  Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglia of Aplysia produce presynaptic facilitation of siphon sensory neurons , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  E. Kandel,et al.  Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia , 1992, Neuron.

[15]  E. Kandel,et al.  Long-term facilitation in Aplysia involves increase in transmitter release. , 1988, Science.

[16]  E R Kandel,et al.  Inhibitor of protein synthesis blocks long-term behavioral sensitization in the isolated gill-withdrawal reflex of Aplysia. , 1989, Journal of neurobiology.

[17]  Eric R. Kandel,et al.  Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation , 1990, Nature.

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

[19]  S. Schacher,et al.  Neurite regeneration by Aplysia neurons in dissociated cell culture: modulation by Aplysia hemolymph and the presence of the initial axonal segment , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  G. A. Clark,et al.  Induction of long-term facilitation in Aplysia sensory neurons by local application of serotonin to remote synapses. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[21]  E. Kandel,et al.  Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia. , 1976, Science.

[22]  S. Schacher,et al.  Synaptic plasticity in vitro: cell culture of identified Aplysia neurons mediating short-term habituation and sensitization , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  E R Kandel,et al.  Neuronal Mechanisms of Habituation and Dishabituation of the Gill-Withdrawal Reflex in Aplysia , 1970, Science.

[24]  S. Schacher,et al.  Selective short- and long-term effects of serotonin, small cardioactive peptide, and tetanic stimulation on sensorimotor synapses of Aplysia in culture , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Perla b. Ephrussi Experimentelle Beiträge zur Lehre vom Gedächtnis , 1904 .

[26]  Irving Kupfermann,et al.  Neuronal Correlates of Habituation and Dishabituation of the Gill-Withdrawal Reflex in Aplysia , 1970, Science.