Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica - PubMed (original) (raw)

Comparative Study

. 1998 Jul-Aug;5(3):246-56.

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Comparative Study

Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica

J Mauelshagen et al. Learn Mem. 1998 Jul-Aug.

Abstract

Serotonin (5HT)-induced facilitation of synaptic transmission from tail sensory neurons (SNs) to motor neurons (MNs) in the marine mollusc Aplysia provides a cellular model of short- and long-term memory for behavioral sensitization of the tail withdrawal reflex. Synaptic facilitation at these synapses occurs in three temporal phases: short-term (STF, lasting minutes), intermediate-term (ITF, lasting more than an hour), and long-term (LTF, lasting >24 hr). STF, ITF, and LTF differ in their induction requirements: A single brief exposure of 5HT induces STF, whereas five applications are required for ITF and LTF. Moreover, STF and LTF can be induced independently. Different forms of memory often show differential sensitivity to the pattern of training trials. To begin to explore this effect at a cellular level, we examined ITF and LTF induced by one of two patterns of 5HT application: a spaced pattern (five 5-min exposures with an interval of 15 min) or a massed pattern (one continuous 25-min application). The spaced and massed patterns both induced ITF; however, spaced 5HT application was significantly more reliable at inducing LTF than was massed application. Thus, whereas induction of ITF and LTF require similar amounts of 5HT, the cellular mechanisms underlying the induction of LTF are more sensitive to the pattern of the induction trials. In the massed group, further analysis revealed a relationship between the expression of ITF and the subsequent expression of LTF, suggesting that these two processes may be mechanistically related.

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Figures

Figure 1

Figure 1

Diagram of experimental protocol for spaced and massed application of 5HT. Three pretests were recorded to establish the baseline EPSP amplitude. 5HT was then applied (solid bars) in one of two patterns: five 5-min pulses (spaced), or one continuous pulse of 25 min (massed). Synapses were tested for the expression of STF (light shading), ITF (medium shading), and LTF (dark shading) at the time points indicated by arrows.

Figure 2

Figure 2

Sample recordings showing EPSP amplitude at representative short-term, intermediate-term, and long-term time points from two preparations that received either spaced (5 × 15 min) or massed (1 × 25 min) application of 5HT. STF, ITF, and LTF were all expressed with both the spaced and massed protocols. In each set of traces, the dashed line represents the baseline EPSP amplitude and the shaded regions (light shading for STF, medium shading for ITF, and dark shading for LTF) indicate change from baseline.

Figure 3

Figure 3

Summary of results. Significant STF and ITF were expressed with either spaced or massed application of 5HT. Significant LTF was expressed in the spaced group but not in the massed group. (*) Significant facilitation from baseline (P < 0.05). For the spaced group (top), from left to right, n = 10, 6, 8, 7, 8, 9, and 10. For the massed group (bottom), n = 9 for all tests except T45, where n = 7.

Figure 4

Figure 4

The probability of inducing LTF is higher with spaced application (n = 10) of 5HT than with massed application (n = 9). Each bar represents the percentage of experiments in which the EPSP amplitude, measured 21 hr after 5HT application, was significantly higher than baseline.

Figure 5

Figure 5

Examples of two preparations that received a massed application of 5HT, one of which expressed LTF (LT+), the other of which did not (LT−). ITF was expressed only in preparations that later expressed LTF. Shading indicates change from baseline (broken line).

Figure 6

Figure 6

LTF expression is associated with ITF expression with massed application of 5HT. Summary graphs of the preparations that received massed application of 5HT, divided into those that expressed LTF (LT+, top) and those that did not (LT−, bottom). Significant ITF was seen only in the group that also expressed LTF. Shading indicates change from baseline at STF (light), ITF (medium), and LTF (dark) time points. Because the two groups were selected according to their T21-hr test score, this point was not included in the statistical analysis. n = 4 (LT+); n = 5 (LT−).

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