Involvement of presynaptic and postsynaptic mechanisms in a cellular analog of classical conditioning at Aplysia sensory-motor neuron synapses in isolated cell culture.
Temporal pairing of presynaptic activity and serotonin produces enhanced facilitation at Aplysia sensory-motor neuron synapses (pairing-specific facilitation), which may contribute to classical conditioning of the gill and siphon withdrawal reflex. This cellular analog of conditioning is thought to involve Ca2+ priming of the cAMP pathway in the sensory neurons. Consistent with that idea, we have found that pairing-specific facilitation by serotonin is greatly reduced by presynaptic injection of a slow Ca2+ chelator or a specific inhibitor of cAMP-dependent protein kinase and is accompanied by a transient increase in the frequency but by no change in the amplitude of spontaneous, miniature EPSPs. However, like post-tetanic potentiation (PTP) and long-term potentiation (LTP) at these synapses, pairing-specific facilitation is also greatly reduced by postsynaptic injection of a rapid Ca2+ chelator or by postsynaptic hyperpolarization during training, although postsynaptic hyperpolarization has no effect on the increase in frequency or on the amplitude of spontaneous EPSPs. These results suggest that pairing-specific facilitation by serotonin involves Hebbian postsynaptic as well as non-Hebbian presynaptic components that interact in some way, perhaps via retrograde signaling, to specifically enhance evoked, synchronized release of transmitter.
Bao
J X
JX
Center for Neurobiology and Behavior, College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA.
Kandel
E R
ER
Hawkins
R D
RD
D000818:Animals; D001048:Aplysia / Q000502:physiology*; D002118:Calcium / Q000502:physiology; D002478:Cells, Cultured; D002614:Chelating Agents / Q000494:pharmacology; D003214:Conditioning, Classical / Q000502:physiology*; D017868:Cyclic AMP-Dependent Protein Kinases / Q000378:metabolism; D004533:Egtazic Acid / Q000031:analogs & derivatives / Q000494:pharmacology; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology; D017774:Long-Term Potentiation / Q000502:physiology; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology; D009046:Motor Neurons / Q000737:chemistry / Q000166:cytology / Q000502:physiology*; D009475:Neurons, Afferent / Q000737:chemistry / Q000166:cytology / Q000502:physiology*; D017729:Presynaptic Terminals / Q000737:chemistry / Q000201:enzymology; D017661:Receptors, Presynaptic / Q000502:physiology*; D012701:Serotonin / Q000494:pharmacology
D002614:Chelating Agents; D017661:Receptors, Presynaptic; D012701:Serotonin; D004533:Egtazic Acid; D017868:Cyclic AMP-Dependent Protein Kinases; C025603:1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid; D002118:Calcium