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. 2006 Feb 15;571(Pt 1):75-82.
doi: 10.1113/jphysiol.2005.100685. Epub 2005 Dec 1.

Synapsin-regulated synaptic transmission from readily releasable synaptic vesicles in excitatory hippocampal synapses in mice

Øivind Hvalby  1 , Vidar Jensen, Hung-Teh Kao, S Ivar Walaas
Affiliations

Synapsin-regulated synaptic transmission from readily releasable synaptic vesicles in excitatory hippocampal synapses in mice

Øivind Hvalby et al. J Physiol. .

Abstract

The effects of synapsin proteins on synaptic transmission from vesicles in the readily releasable vesicle pool have been examined by comparing excitatory synaptic transmission in hippocampal slices from mice devoid of synapsins I and II and from wild-type control animals. Application of stimulus trains at variable frequencies to the CA3-to-CA1 pyramidal cell synapse suggested that, in both genotypes, synaptic responses obtained within 2 s stimulation originated from readily releasable vesicles. Detailed analysis of the responses during this period indicated that stimulus trains at 2-20 Hz enhanced all early synaptic responses in the CA3-to-CA1 pyramidal cell synapse, but depressed all early responses in the medial perforant path-to-granule cell synapse. The synapsin-dependent part of these responses, i.e. the difference between the results obtained in the transgene and the wild-type preparations, showed that in the former synapse, the presence of synapsins I and II minimized the early responses at 2 Hz, but enhanced the early responses at 20 Hz, while in the latter synapse, the presence of synapsins I and II enhanced all responses at both stimulation frequencies. The results indicate that synapsins I and II are necessary for full expression of both enhancing and decreasing modulatory effects on synaptic transmission originating from the readily releasable vesicles in these excitatory synapses.

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Figures

Figure 1
Figure 1. Unchanged Ca2+ dependencies of synaptic strength and of presynaptic volley amplitudes in control and DKO mice
A, normalized increase in the mean field EPSP slope following equilibration (60 min) from 1 mm to 2 mm (left columns, 1–2) and from 2 mm to 4 mm Ca2+ (right columns, 2–4) in wild-type (WT; open columns, n = 12 and n = 19, respectively) and double knock-out (DKO; filled columns, n = 10 and n = 16, respectively) mice. Vertical bars indicate s.e.m.B, presynaptic volley amplitudes as a function of stimulus number during 20 Hz stimulation (2 mm Ca2+) in wild-type (○, n = 13) and DKO (•, n = 6) mice. Experiments were done in the presence of 50 µm APV and 10 µm CNQX. Vertical bars indicate s.e.m.
Figure 2
Figure 2. Synaptic strength in the CA3–CA1 synapse as a function of stimulus number during repetitive stimulation in wild-type mice
The graphs show the synaptic strength at different frequencies and at different [Ca2+]o. The inset in A shows superimposed synaptic responses in 2 mm Ca2+ at the times indicated by arrows and numbers. A, normalized and pooled field EPSP values in wild-type mice at 20 Hz stimulation in the presence of 1 mm (red circles, n = 12), 2 mm (blue circles, n = 22) and 4 mm Ca2+ (green triangles, n = 11). B–D, as in A but at 10 Hz (n = 13, n = 20 and n = 11), 5 Hz (n = 11, n = 12 and n = 10) and 2 Hz (n = 10, n = 10 and n = 10) stimulation, respectively. Vertical bars indicate s.e.m.
Figure 3
Figure 3. Synaptic strength in the CA3–CA1 synapse as a function of stimulus number during repetitive stimulation in DKO mice
The graphs show the synaptic strength at different frequencies and at different [Ca2+]o. The inset in A shows superimposed synaptic responses in 2 mm Ca2+ at the times indicated by arrows and numbers. A, normalized and pooled field EPSP values in wild-type mice at 20 Hz stimulation in the presence of 1 mm (red circles, n = 12), 2 mm (blue circles, n = 18) and 4 mm Ca2+ (green triangles, n = 10). B–D, as in A, but at 10 Hz (n = 10, n = 16 and n = 10), 5 Hz (n = 10, n = 9 and n = 10) and 2 Hz (n = 9, n = 12 and n = 9) stimulation, respectively. Vertical bars indicate s.e.m.
Figure 4
Figure 4. Synaptic strength in the CA3–CA1 synapse as a function of stimulus number during 20 Hz stimulation in wild-type and DKO mice in the presence of 2 mm Ca2+
Normalized and pooled intracellularly recorded EPSP values in wild-type mice (A) and DKO mice (B). Vertical bars indicate s.e.m., n = 17 (wild-type) and 11 (DKO).
Figure 5
Figure 5. Frequency-dependent switch in the function of synapsins in the CA3–CA1 synapse
A, subtraction of the values obtained at different frequencies in DKO mice (Fig. 3) from those obtained in wild-type (Fig. 2) at 1 mm Ca2+. The frequency 20 Hz is symbolized by dark blue circles, 10 Hz by yellow circles, 5 Hz by orange circles and 2 Hz by turquoise circles. B–C, as in A, but at 2 mm and 4 mm Ca2+, respectively. D, subtraction of the intracellular EPSP values obtained by intracellular recordings at 20 Hz stimulation at 2 mm Ca2+ in DKO mice (Fig. 4B) from those in wild-type mice (Fig. 4A). Horizontal bars along the abscissa with colours corresponding to the respective frequencies indicate P < 0.05 when comparing the results from wild-type and DKO mice (Figs 2 – 4).
Figure 6
Figure 6. Synaptic strength in the medial perforant path-to-granule cell synapse as a function of stimulus number during repetitive stimulation in 2 mm CaCl2
The graphs show synaptic strength in 2 mm Ca2+ at 20 Hz (upper panel) and 2 Hz (lower panel) in wild-type (○) and DKO mice (•). Subtraction of the values obtained at 20 Hz and 2 Hz in DKO mice from those obtained in wild-type is represented by ▵. A, normalized and pooled field EPSP values in wild-type (n = 16) and DKO (n = 17) mice at 20 Hz stimulation. The insets show synaptic responses in 2 mm Ca2+ superimposed at the stimulation times indicated by numbers. B, as in A, but at 2 Hz stimulation frequency. Vertical bars indicate s.e.m., n = 16 in both genotypes. Horizontal, filled bars along the abscissa indicate P < 0.05 when comparing the results from the two genotypes.
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