Parallel somatic and synaptic processing in the induction of intermediate-term and long-term synaptic facilitation in Aplysia - PubMed (original) (raw)

Parallel somatic and synaptic processing in the induction of intermediate-term and long-term synaptic facilitation in Aplysia

Carolyn M Sherff et al. Proc Natl Acad Sci U S A. 2004.

Abstract

The induction of different phases of memory depends on the amount and patterning of training, raising the question of whether specific training patterns engage different cellular mechanisms and whether these mechanisms operate in series or in parallel. We examined these questions by using a cellular model of memory formation: facilitation of the tail sensory neuron-motor neuron synapses by serotonin (5-hydroxytryptamine, 5-HT) in the CNS of Aplysia. We studied facilitation in two temporal domains: intermediate-term facilitation (1.5-3 h) and long-term facilitation (LTF, >24 h). Both forms can be induced by using several different temporal and spatial patterns of 5-HT, including (i) repeated, temporally spaced pulses of 5-HT to both the sensory neuron soma and the sensory neuron-motor neuron synapse, and (ii) temporally asymmetric exposure of 5-HT to the soma and synapse under conditions in which neither exposure alone induces LTF. We first examined the protein and RNA synthesis requirements for LTF induced by these two patterns and found that asymmetric (but not repeated) 5-HT application induced LTF that required postsynaptic protein and RNA synthesis. We next focused on the patterning and protein synthesis requirements for intermediate-term facilitation. We found that intermediate-term facilitation (i) is induced locally at the synapse, (ii) requires multiple pulses of 5-HT, and (iii) requires synaptic protein synthesis. Our findings show that different temporal and spatial patterns of 5-HT induce specific temporal phases of long-lasting facilitation in parallel by engaging different cellular and molecular mechanisms.

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Figures

Fig. 1.

Fig. 1.

LTF induced by asymmetric 5-HT requires postsynaptic protein synthesis, whereas LTF induced by repeated 5-HT does not. (A) Diagram of recordings in the two-compartment chamber. Protein synthesis was blocked in one MN by injection of gelonin; the other MN received a control injection. (B and C) Gelonin blocked induction of LTF by asymmetric 5-HT (B, n = 9) but not by repeated pulses of 5-HT (C, n = 8). [Scale bar, 20 ms, 10 mV (MNs), 36 mV (SN).] *, P < 0.05.

Fig. 2.

Fig. 2.

LTF induced by symmetric 5-HT requires both presynaptic and postsynaptic gene expression. (A) Treatment of either the somatic or synaptic compartment with the transcription blocker actinomycin D blocked the induction of LTF (n = 3 in each group). (B) LTF was also blocked when transcription in the synaptic compartment was reversibly blocked with DRB (5-HT + DRB, n = 5) compared with 5-HT alone (5-HT, n = 6). *, P < 0.05.

Fig. 3.

Fig. 3.

ITF induced at the synapse requires local protein synthesis. (A) Both STF (n = 7) and ITF (n = 8) were induced by repeated synaptic 5-HT, whereas neither was induced by repeated somatic 5-HT (n = 7 in each group). LTF was induced by both synaptic 5-HT (n = 5) and somatic 5-HT (n = 6). (B) ITF induced by repeated 5-HT (n = 5) was blocked by emetine at the synapse (n = 6). STF was induced in both groups (5-HT, n = 5; 5-HT + emetine, n = 6), and LTF (5-HT, n = 5; 5-HT + emetine, n = 3) was unaffected. *, P < 0.05.

Fig. 4.

Fig. 4.

Asymmetric 5-HT does not induce ITF. Asymmetric 5-HT (n = 13) and repeated-pulse 5-HT (n = 11) induced similar STF, but only repeated-pulse 5-HT (n = 9) induced ITF. Asymmetric 5-HT (n = 10) actually induced depression. *, P < 0.05.

Fig. 5.

Fig. 5.

Four different spatial patterns of 5-HT produce distinct temporal phases of synaptic facilitation. (A and B) Repeated pulses of 5-HT to both the somatic and synaptic compartments (A) or to only the synaptic compartment (B) induce all three phases of facilitation: STF, ITF, and LTF. (C) Repeated pulses of 5-HT only to the soma induce LTF in the absence of STF and ITF. (D) Asymmetric 5-HT induces STF and LTF but not ITF. Hatched shading, local induction at the synapse; cross-hatched shading, protein synthesis-dependent local induction at the synapse; vertical stripes, protein and RNA synthesis-dependent local induction at the synapse.

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