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Research Articles, Systems/Circuits

Single Bursts of Individual Granule Cells Functionally Rearrange Feedforward Inhibition

Máté Neubrandt, Viktor János Oláh, János Brunner, Endre Levente Marosi, Ivan Soltesz and János Szabadics
Journal of Neuroscience 14 February 2018, 38 (7) 1711-1724; DOI: https://doi.org/10.1523/JNEUROSCI.1595-17.2018
Máté Neubrandt
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary,
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Viktor János Oláh
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary,
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János Brunner
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary,
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Endre Levente Marosi
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary,
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Ivan Soltesz
2Department of Neurosurgery, and
3Stanford Neurosciences Institute, Stanford University, Stanford, California 94305
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János Szabadics
1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary,
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  • Figure 1.
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    Figure 1.

    Single, brief MF bursts potentiate monosynaptic MF-EPSCs in CA3 FF-INs for several seconds. A, Schematic representation of the recording configuration for unitary MF responses in CA3 neurons. Presynaptic patch-clamp recording was obtained from a single giant MF terminal (most of these originate from DG GCs; Fig. 1-1) or a single CA3 GC (somatic recording; these cells are rarer but easier to record than the MF terminals); the postsynaptic cell was an FF-IN. MF output was first measured with a control stimulus, followed by a single 2–20 AP burst (150 Hz); after various time delays (0.1–13.5 s), which approximated the typical physiological inactivity periods in GCs in vivo, a test response was evoked. Right, Example traces of single-AP-evoked control and test EPSCs in an identified FF-IN (the illustrated recordings were from an IvyC; for the anatomy of the presynaptic and postsynaptic cells, see Fig. 1-1). In most cases, control and test pulses contained 3 APs at 20 Hz to gain insight into possible changes in short-term plasticity after the bursts; plots in this and subsequent figures show responses to the first APs in the triplet, except in Figure 4C, D. B, Time course of the relative amplification of monosynaptic MF-EPSCs after single 15 AP presynaptic bursts in the same individual MF. Relative postburst EPSC amplitudes are shown (i.e., control relative amplitudes are 1, dashed line). The x axis indicates the time of the test pulse after the burst. The graph includes all data points (n = 280, first APs) from identified FF-IN pairs (n = 78 pairs; including IvyCs: n = 55 pairs; AACs: n = 10; PV+BC: n = 5; CCK+IN, n = 8; for separate analysis of the burst-induced amplification in different postsynaptic cell types, see Figs. 1-1, 1-2, 1-3, and 1-4). Insets, Example test responses in blue at different postburst delays; same postsynaptic IvyC as in A; control traces are black. C, Dependence of the postburst potentiation on AP numbers within the burst (from n = 99 data points from n = 28 pairs). Brown curve indicates the exponential fit of the data (R2 = 0.966). Gray area represents the typical range of GC bursts in vivo. Insets, Example test and control traces and the time course of the changes of the responses after 3, 5, 9, and 15 AP bursts. D, Effects of single presynaptic bursts consisting of 8 APs at 20, 40, 80, and 150 Hz, on the same MF-FF-IN pairs (n = 7). E, Effects of single bursts, whose patterns were obtained from in vivo recorded identified GCs: #1, 6 APs with 3.7, 7.5, 4.54, 6.98, and 5.88 ms interspike intervals (Henze et al., 2002); #2, 4 APs with 4, 6, and 9 ms interspike intervals (Pernía-Andrade and Jonas, 2014); #3, 5 APs with 6, 8, 11, and 15 ms interspike intervals (Diamantaki et al., 2016); for comparison, the effect of a 6 AP 150 Hz burst is also shown. The effects were measured with each realistic burst protocol in the same pairs (n = 8 pairs, 3.6 s after burst).

  • Figure 2.
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    Figure 2.

    Postsynaptic cell type specificity of postburst potentiation of MF-EPSCs. A, Single presynaptic MF bursts, consisting of various numbers of APs, resulted in small postburst potentiation effects on the EPSCs of a representative MF-pyramidal cell pair. Traces represent presynaptic MF terminal APs in bouton-attached recordings (gray) and the postsynaptic responses before and after single burst. Bursts and postsynaptic responses (including preburst control and postburst test EPSCs, and during-burst responses) are shown next to the corresponding traces. B, Time course of the effects of single, brief presynaptic bursts (6 or 15 AP, 150 Hz) on subsequent single-AP-evoked MF-EPSCs in postsynaptic CA3 pyramidal cells (n = 46 data points from n = 12 pairs; compare with Fig. 1B). Inset, Example control and test MF responses at different postburst delays. Anatomy of the postsynaptic pyramidal cell and presynaptic DG GC (back-labeled via the MF terminal recording) is shown in Figure 2-1. C, Summary graph showing the amplitude of the postburst test responses in pyramidal cells and FF-INs relative to the compound maximal amplitudes reached during the bursts (dashed line) in the same synaptic inputs (red represents pyramidal cells, n = 46 data points from n = 12 pairs; blue represents FF-INs with 15 AP bursts; light blue represents FF-INs with short, 3 or 5 AP bursts, n = 10 pairs; the same responses were reanalyzed as in Fig. 1B,C). The relative amplitudes of the preburst control responses (“before”) are shown separately. D, Comparison of MF-EPSCs before, during, and after single presynaptic MF bursts in a representative FF-IN (blue traces) and pyramidal cell (red). Green dashed lines indicate maximum amplitude of the compound EPSCs during the burst for comparison. Gray areas represent the integral areas (charge transfer). Bottom, Graphs represent the activity- and postsynaptic cell type-dependent differences of the time course of charge transfer.

  • Figure 3.
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    Figure 3.

    Effects of single MF bursts on the unitary MF responses evoked in SLCs, which are GABAergic but are not considered to be FF-INs. A, Control and postburst test MF-EPSCs from an example CA3 GC-SLC pair at three different time points after single presynaptic bursts. Gray bars represent APs, often weak responses among the frequent spontaneous events. B, The MF responses of two SLCs during the burst (15 APS at 150 Hz) in standard solutions (top) and in the presence of presynaptic intracellular CsCl (by replacing 40 mm KCl) and 3.5 mm extracellular Ca2+ level (bottom, **). C, A representative experiment, in which reliable synaptic transmission was obtained in a CA3 GC-to-SLC connection by the above modifications in the recording conditions. D, Summary graph showing the amplitude of the postburst responses in SLCs relative to the compound maximal amplitudes during the bursts. Dark blue represents SLC with standard presynaptic recording (n = 61 data points from n = 20 pairs). Gray represents SLC with artificially elevated MF release (n = 15 data points from n = 5 pairs). Blue curve indicates data for FF-INs replotted from Figure 2C to highlight the robust differences between the two GABAergic cell groups. The relative amplitudes of the control responses before the bursts are shown separately. For the anatomy of the presynaptic and postsynaptic cells, see Figure 3-1.

  • Figure 4.
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    Figure 4.

    Presynaptic origin of the burst-induced potentiation in FF-INs. A, The probability of synaptic response failures decreases after single presynaptic MF bursts. Representative traces of a CA3 GC-CCK+ basket cell connection before (black) and after (blue) single bursts (10 traces from each condition). Right, Connected gray symbols represent the failure rates in individual pairs with identified FF-INs (n = 68 pairs) during control and test MF stimuli (1.5–6.7 s postburst delays). Black represents the average data from all FF-IN connections. The failure rates were analyzed from at least 10 trials for each condition. B, Actual and normalized average EPSCs evoked in FF-INs (n = 51 pairs) by single MF APs before and 1.5–6.7 s after single presynaptic bursts. The events were aligned to the presynaptic AP peak. Graphs represent the half-width and 10%–90% rise times of the MF responses in individual FF-INs (gray) and their average (black), which were similar before and after the bursts. C, Example traces demonstrating changes in short-term plasticity of the MF-EPSCs in an IvyC evoked by 3 APs before and 6 s after bursts (control PPR: 1.26; test PPR: 0.45). Summary plot shows data from all in identified postsynaptic FF-INs; the PPR (calculated as the ratio of the average of the second and third amplitudes to the first amplitude) was low during the time when the EPSCs were potentiated. Summary bar graphs represent PPRs of all FF-IN connections before (control) and 1.5–6.7 s after the burst (test). D, Example traces: from IvyC MF pairs; note the similarity of test PPRs (at 6 s postburst) despite the different control PPRs. Right panels: Top, Correlation between the control (initial) PPR and the magnitude of potentiation (linear fit, maroon line; note the logarithmic scaling of the PPR axes). Bottom, Independence of postburst test PPR of the control PPR. Each circle represents individual test responses from identified FF-IN pairs. Circles with gray fillings indicate the representative pairs illustrated in C and D. * marks significant difference between control and test responses (see text for details).

  • Figure 5.
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    Figure 5.

    Investigations into mechanisms of postburst plasticity in FF-INs. A, Persistence of the postburst potentiation in lower (1.3 mm; allegedly physiologically more relevant) extracellular Ca2+ levels. Example traces are shown from a CA3 GC-IvyC pair in which the effects of single presynaptic bursts were first tested in the presence of standard 2 mm Ca2+ concentrations and then in 1.3 mm Ca2+ (preburst control responses: black; test responses: blue, 3.6 s after burst). Bar graphs represent average data from all pairs (n = 8); the lower Ca2+ concentration decreased the response amplitudes and increased the PPRs, but the potentiation persisted. B, Example traces from a CA3 GC-AAC pair in which the effects of single presynaptic bursts were tested while the presynaptic CA3 GC was recorded with 1 mm intracellular EGTA to chelate Ca2+. Bar graphs represent average data from all presynaptic EGTA pairs (n = 8). Presynaptic EGTA strongly decreased the control responses, but the burst-induced potentiation persisted. C, Example traces illustrate the accelerated and more precise release before and after single presynaptic bursts from the same pair; average presynaptic APs and individual EPSCs are shown; mean and variance of the delay are also indicated, with error bars; failures were excluded for clarity. Right panels, Plots of the mean and variance values of the synaptic onset delay in each MF-FF-IN pair before and after single bursts (connected gray symbols) and their average (black). D, The DAG analog phorbol ester PDBu (1 μm), which promotes vesicle priming, increased MF-EPSC amplitude before bursts (note the different scale bars) and prevented burst-induced potentiation in a representative pair. Subsequent reduction of the release probability following the application of decreased extracellular Ca2+ (1 mm) in the PDBu-containing perfusing solution significantly reduced the average amplitudes, but burst-induced amplification remained negligible in the same pair. Summary bar graphs show that bursts were no longer effective in eliciting potentiation in the same pairs in the presence of PDBu regardless of the release probability; furthermore, PDBu also prevented the burst-induced decrease in the delay of the responses (bottom right). Symbols represent changes in synaptic delays in control conditions and in the presence of PDBu. Bars represent average data. * marks significant difference.

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    Figure 6.

    Summary of the pharmacological experiments aimed at probing the potential involvement of various plasticity pathways in the postburst potentiation in FF-INs. A, Calphostin-C (1 μm, n = 12) is a PKC (and Munc13) inhibitor that acts on DAG-binding domains. U73122 (2.5 μm, n = 8) is a phospholipase C inhibitor. Both inhibitors affected baseline release as indicated by the attenuation of the control response amplitudes indicating the involvement of these pathways in the regulation of release at these synapses, serving as positive internal controls indicating drug effectiveness. PKC19-36 (100 μm, n = 7, synthetic autoinhibitory domain, applied intracellularly) and GF109203X (1 μm, n = 11, acts on the ATP binding site; slices were preincubated for at least 60 min) are selective PKC inhibitors. The small control amplitudes and large PPRs provided positive internal controls for these inhibitors. The averages of all control responses are also shown for comparison (because these inhibitors required intracellular application and pretreatment). DCG IV is an mGluR2/3 agonist (1 μm, n = 7) that selectively inhibits MF responses. * marks significant difference in the control (before burst) EPSC amplitudes in control conditions and after drug application. B, Average amplification at 1.5–6.7 s after single 15 AP bursts in the presence of various pharmacological agents. In addition to the above drugs, the burst-induced amplification of MF-EPSCs is shown in the presence of Go6976 (0.25 μm, n = 8, a subtype-selective PKC inhibitor), KT5720 (200 nm, n = 10, a PKA inhibitor that works by competing with ATP binding; PKAs are involved in pathways that regulate presynaptic release, including RIM proteins, whose PKA-dependent phosphorylation promotes vesicle priming and PKAs are also involved in posttetanic potentiation mechanisms at MF synapses onto DG inhibitory cells) (Alle et al., 2001), PKI (2.5 μm intracellularly, PKA inhibitory fragment 6–22 amide, that binds to the substrate site) (Hashimotodani et al., 2017), AMN082 (1 μm, n = 6, selective mGluR7 agonist), MSOP (150 μm, n = 8, selective inhibitor of Group III mGluRs including mGluR7), or BINA (5 μm, n = 12, selective positive allosteric modulator of mGluR2). For additional positive control effects, see Results. Postburst potentiation in the absence of these drugs (“control amplification”) is also shown for comparison. None of these pharmacological modifiers of known plasticity pathway components was able to significantly block the postburst potentiation.

  • Figure 7.
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    Figure 7.

    Differential effects of single bursts in individual MFs on diIPSCs and diEPSCs. A, Example traces: Synaptic events in a single randomly chosen CA3 pyramidal cell during the stimulation of a simultaneously recorded single CA3 GC that was not monosynaptically connected to the pyramidal cell; the majority of the outward events are disynaptic GABAergic responses (diIPSCs; at −50 mV using low chloride internal solution in postsynaptic cells), which presumably originate from one or more nonrecorded FF-IN(s); there is increased probability of diIPSC after single bursts in the MF (test). Black average traces represent the increased weight of disynaptic inhibition after the bursts. Right, Bar graphs represent summary data from diIPSC experiments. The bar graphs illustrate two types of diIPSC pairs: one in which the presynaptic MF source was a MF terminal (presumably originating from DG GCs), the other in which the MF source was a somatically recorded CA3 GC. There is a lack of differences in the burst-induced changes in the diIPSCs, suggesting that these two MF recording configurations induce similar burst-dependent effects on the CA3 feedforward inhibitory circuit. B, Summary data indicating that the postburst time course of the increase in the probability of single MF-evoked diIPSCs. There is similarity of the time course to that of the burst-induced potentiation of the MF-EPSCs in FF-INs in Figure 1B. The increase in the probability of the diIPSCs during the burst (dark blue) was smaller than it was after the burst, consistent with the FF-IN data in Figure 2C. C, Example traces: diEPSC events recorded from a nonidentified fast-spiking interneuron during the activation of a CA3 GC; these diEPSCs presumably reflect the spiking of one or more nonrecorded pyramidal cell(s); there are frequent diEPSCs during the high-frequency bursts (inset), whereas the probability of diEPSCs remained unchanged after the bursts. D, Summary data: burst effects on the probability of diEPSCs evoked by MFs before, during (bars), and after bursts in the same individual MF (average data of 6 pairs, with 15 AP bursts at 150 Hz); note the difference compared with the data in B, and the similarity to the MF-EPSC pyramidal cell data in Figure 2C. * mark significant difference in the probability of disynaptic events relative to control probabilities (before burst). E, Distribution of the onset time delays of individual postsynaptic events measured from the time of the presynaptic AP, including monosynaptic EPSCs in postsynaptic FF-INs (gray), diIPSCs in CA3 pyramidal cells (blue), and diEPSCs in GABAergic cells (red). The 10%–90% rise time and decay time constants of the diIPSCs and diEPSCs are shown below. Each data point represents an individual pair.

Extended Data

  • Figures
  • Figure 1-1

    Postsynaptic Ivy cells (IvyC): Morphological identification, comparison with the pooled data from all FF-INs and representative MF terminal (presynaptic DG GC) to IvyC and CA3 GC to IvyC pairs. A, Upper panel: firing pattern of the presynaptic MF terminal; lower: example traces show the presynaptic AP in the MF terminal and the EPSC response in the IvyC. B, Back-labeled parent GC soma (B1) in the DG following the recording of the presynaptic MF terminal in the CA3; and MF terminals (B2) along the recorded axon. C, Axon morphology (C1) and immunohistochemical testing (C2) of the postsynaptic IvyC in the stratum radiatum of the CA3. The inset shows the firing pattern of the IvyC. D, Control and post-burst test MF-EPSCs from the example MF bouton-IvyC pair, 8.4 seconds after the burst (15 AP at 150 Hz). E, Comparison of the amplification of the MF responses from IvyC pairs (n = 55) with the pooled FF-IN data (see Fig. 1B). The insets show the control (before burst) and four different delays after the single bursts from the pair shown in panel D. F-G, Identification of the presynaptic CA3 GC and the postsynaptic IvyC shown in Fig. 1A-B. F, The presynaptic CA3 GC and the postsynaptic IvyC are marked by gray and blue asterisks, respectively. G, Characteristic dendritic morphology (left) with spines (right, top) and large MF terminals (right) of the CA3 GC. H, Axons of the postsynaptic IvyC in the stratum radiatum of the CA3. I, Firing patterns of the cells. J, Individual data points from all the FF-IN pairs (together with the average data), illustrating the time course of the post-burst potentiation. Download Figure 1-1, PDF file

  • Figure 1-2

    Postsynaptic axo-axonic cells (AAC): Morphological identification and comparison with the pooled data from all FF-INs. A, Control and post-burst test MF-EPSCs from an example CA3 GC-AAC pair, 3.5 seconds after the burst. B, Comparison of the amplification of the MF responses from AAC pairs (n = 10) with the pooled FF-IN data (see Fig. 1B). The relative post-burst EPSC amplitudes are shown as in Fig. 1B (i.e., control relative amplitudes are 1, dashed line). The insets show the control (before burst) and three different delays after single bursts. C, Axons of the postsynaptic AAC at the border of strata pyramidale and oriens. The MF that originated from the presynaptic CA3 GC is visible at the border of strata lucidum and pyramidale. The inset shows the fast-spiking properties of the postsynaptic AAC. D, Immunolabeling for PV and SATB1 (negative) of the postsynaptic AAC (Viney et al., 2013). E, Firing pattern and stratum radiatum dendrites of the presynaptic CA3 GC. Download Figure 1-2, PDF file

  • Figure 1-3

    Postsynaptic CCK-expressing interneurons (CCK+IN): Morphological identification and comparison with the pooled data from all FF-INs. A, Control and post-burst test MF-EPSCs from an example CA3 GC-CCK+IN pair 4.5 seconds after the burst. B, Comparison of the amplification of the MF responses from CCK+IN pairs (n = 8) with the pooled FF-IN data (see Fig. 1B). The relative post-burst EPSC amplitudes are shown as in Fig. 1B (i.e., control relative amplitudes are 1, dashed line). The insets show the control (before burst, black) and test responses (blue) at four different delays after the single bursts. C, The presynaptic CA3 GC and the postsynaptic CCK+IN (a basket cell) are highlighted by gray and blue asterisks, respectively. D, Immunolabeling for CCK and SATB1 (negative) of the postsynaptic cell. E, Dendrites of the presynaptic CA3 GC. F, Firing patterns of the pre- and postsynaptic cells. Download Figure 1-3, PDF file

  • Figure 1-4

    Postsynaptic PV-expressing basket cells (PV+BC): Morphological identification and comparison with the pooled data from all FF-INs. A, Control and post-burst test MF-EPSCs from an example CA3 GC-PV+BC pair 5 seconds after the burst. B, Comparison of the post-burst potentiation of the MF responses from PV+BC pairs (n = 10) with the pooled FF-IN data (see Fig. 1B). The relative post-burst EPSC amplitudes are shown as in Fig. 1B (i.e., control relative amplitudes are 1, dashed line). C, Basket axons, dendrites and firing pattern of the postsynaptic PV+BC. D, Firing pattern of the presynaptic CA3 GC. E, Immunolabeling for PV in the dendrites of the postsynaptic cell. Download Figure 1-4, PDF file

  • Figure 2-1

    Postsynaptic pyramidal cells: Morphological identification. A, Two recorded pyramidal cells within the CA3, from which the left cell (asterisk) was the postsynaptic partner in the connections shown in Fig. 2A. The insets show the cell body of the postsynaptic pyramidal cell from the neighboring section and the firing pattern of the postsynaptic pyramidal cell. B, Following the cell-attached presynaptic terminal recording, the presynaptic MF terminal was loaded with biocytin in whole-cell mode, enabling the visualization of the parent GC soma in the DG and typical large MF terminals along its axon (insets). Download Figure 2-1, PDF file

  • Figure 3-1

    Postsynaptic spiny lucidum cells (SLC): Morphological identification. A, Firing patterns of the presynaptic CA3 GC and postsynaptic SLC in Fig. 3A. B, Dendritic morphology of the two cells at low magnification. C, Dendritic spines of the postsynaptic SLC within the stratum lucidum. D, Immunolabeling of the postsynaptic SLC for somatostatin and CCK (negative). E, Immunolabeling for somatostatin in the postsynaptic SLC from the pair in Fig. 3C. F, Firing patterns of the presynaptic CA3 GC and the postsynaptic SLC in Fig. 3C. G, Nomarski DIC image of the DAB-stained presynaptic CA3 GC and postsynaptic SLC. The inset shows the spiny dendrites of the SLC. Download Figure 3-1, PDF file

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Journal of Neuroscience
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14 Feb 2018
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Single Bursts of Individual Granule Cells Functionally Rearrange Feedforward Inhibition
Máté Neubrandt, Viktor János Oláh, János Brunner, Endre Levente Marosi, Ivan Soltesz, János Szabadics
Journal of Neuroscience 14 February 2018, 38 (7) 1711-1724; DOI: 10.1523/JNEUROSCI.1595-17.2018

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Single Bursts of Individual Granule Cells Functionally Rearrange Feedforward Inhibition
Máté Neubrandt, Viktor János Oláh, János Brunner, Endre Levente Marosi, Ivan Soltesz, János Szabadics
Journal of Neuroscience 14 February 2018, 38 (7) 1711-1724; DOI: 10.1523/JNEUROSCI.1595-17.2018
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