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. 1998 Sep 29;95(20):12004-9.
doi: 10.1073/pnas.95.20.12004.

Target cell-specific modulation of transmitter release at terminals from a single axon

M Scanziani  1 , B H Gähwiler, S Charpak
Affiliations

Target cell-specific modulation of transmitter release at terminals from a single axon

M Scanziani et al. Proc Natl Acad Sci U S A. .

Abstract

In the hippocampus, a CA3 pyramidal cell forms excitatory synapses with thousands of other pyramidal cells and inhibitory interneurons. By using sequential paired recordings from three connected cells, we show that the presynaptic properties of CA3 pyramidal cell terminals, belonging to the same axon, differ according to the type of target cell. Activation of presynaptic group III metabotropic glutamate receptors decreases transmitter release only at terminals contacting CA1 interneurons but not CA1 pyramidal cells. Furthermore, terminals contacting distinct target cells show different frequency facilitation. On the basis of these results, we conclude that the pharmacological and physiological properties of presynaptic terminals are determined, at least in part, by the target cells.

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Figures

Figure 1
Figure 1
L-AP4 reduces EPSCs recorded from interneurons in CA1 but not field EPSPs. Current and voltage traces: Data from a representative experiment in which field and whole-cell recordings were performed simultaneously. Each trace represents the average of 10–20 sweeps. (Lower) Summary graph of the action of L-AP4 (10 μM) on the amplitude of evoked AMPA receptor-mediated EPSCs recorded from CA1 interneurons voltage clamped at −70 mV (n = 11, •). Note the increase of the normalized PPR of the EPSCs recorded from interneurons upon perfusion of L-AP4 (○, bin size: 10 stimuli; the PPR was defined as (p2/p1) where p1 and p2 are the amplitude of the first and second EPSC, respectively). fEPSPs were monitored simultaneously by placing an extracellular-recording pipette in the stratum radiatum in six experiments (▴). No change in PPR could be detected in the field recordings (▵).
Figure 2
Figure 2
(A) Synaptic transmission at Schaffer collateral/interneuron synapses is decreased by L-AP4. (A1) Potassium puffs (2 × 75 ms, 50 ms interval, arrow) applied every 30 s to the surface of the CA3 stratum pyramidale evoked a burst of α-amino-3-hydroxy-5-methyl-4-isoxalozolepropionic acid receptor-mediated EPSCs in a CA1 interneuron voltage- clamped at −70 mV. After bath-application of NBQX (10 μM) the neuron was voltage clamped at +40 mV to record NMDAR-mediated EPSCs. Application of L-AP4 (15 μM) reversibly reduced NMDAR-mediated EPSCs. The current traces are composed of two superimposed sweeps. Lower traces: charge transfer of the current traces illustrated above. (A2). Summary graph of four similar experiments. (B) L-AP4 reduces feed-forward inhibition. Threshold extracellular stimulation in CA3 evoked an EPSP-IPSP sequence in a CA1 pyramidal cell recorded in current-clamp mode (membrane potential manually clamped at −55 mV). The voltage traces represent the average of 20 sweeps. L-AP4 (50 μM) reduced the amplitude of IPSPs but not the slope of EPSPs. Note that NBQX (10 μM) abolished the EPSP and the IPSP. (Inset) Comparison of the action of L-AP4 on IPSPs (i) and EPSPs (e) for the four experiments where a depression of the IPSP was observed.
Figure 3
Figure 3
L-AP4 differentially affects transmitter release from terminals arising from an individual axon that contacts different cell types. (A) Voltage and current traces: action potentials triggered by intracellular current pulses in a presynaptic CA3 pyramidal cell (1) evoked unitary EPSCs in a monosynaptically connected alveus-oriens interneuron (2). L-AP4 (50 μM) reversibly depressed the response. The monosynaptic response between the same presynaptic pyramidal cell and a subsequently recorded postsynaptic pyramidal cell (3) was not affected by L-AP4. The traces are composed of five superimposed sweeps. Plots: time course of this experiment for the amplitudes of the EPSCs; (Insets) EPSC latency histograms. (B) Summary graphs (n = 3; bin size: 3 stimuli). In one experiment, the postsynaptic cells were recorded in the reverse order.
Figure 4
Figure 4
Terminals originating from an individual axon but contacting different cell types display different PPR. (A) Voltage and current traces: action potentials triggered by intracellular current pulses in a presynaptic CA3 pyramidal cell (1) evoked unitary EPSCs in a monosynaptically connected alveus-oriens interneuron (2) and a subsequently recorded pyramidal cell (3). The traces are composed of seven superimposed sweeps. (B) Histogram: Summary graph (n = 3). PPR is p2/p1. (In, interneurons; Pyr, pyramidal cells) (C) Micrograph of a typical Lucifer yellow filled oriens/alveus interneuron in culture. The horizontally extending dendrites run parallel to the stratum pyramidale (Upper) and to the alveus (Lower). (Bar = 60 μm.)
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