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Articles, Cellular/Molecular

Granule Cells in the CA3 Area

János Szabadics, Csaba Varga, János Brunner, Kang Chen and Ivan Soltesz
Journal of Neuroscience 16 June 2010, 30 (24) 8296-8307; DOI: https://doi.org/10.1523/JNEUROSCI.5602-09.2010
János Szabadics
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Csaba Varga
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János Brunner
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Kang Chen
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Ivan Soltesz
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    Figure 1.

    Colocalization of GC markers in a subpopulation of cells in the CA3. A, Low-magnification confocal image of CB (top) and Prox1 (middle; Prox1 immunostaining is restricted to the nuclei of positive cells) immunoreactivity. The bottom panel shows the superimposed images of the CB and Prox1 immunostainings (scale bar, 100 μm; asterisks mark MFs in the CA3 area). B, Some CA3 cells are positive to both CB and Prox1 (horizontal arrows). Note the cells immunopositive for CB only (vertical arrowhead). Note also that dendrite-like, CB-positive processes emerge only from the apical side of double-positive cells, whereas CB-positive but Prox1-negative cells have different multipolar somata (scale bar, 20 μm). C, CB and Prox1 staining of DG GCs.

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    Figure 2.

    Morphology and firing properties of CA3 GCs. A, Whole-cell recorded, biocytin filled, and subsequently reconstructed CA3 GC. A1, Dendritic and axonal arborizations of a CA3 GC (DG, GC layer of the inner blade of the DG; s.rad., stratum radiatum; s.luc., stratum lucidum; s.pyr., stratum pyramidale). The black dot in the inset indicates the location of the soma of the recorded cell within the hippocampus. Note the presence of large (“giant”) terminals with filopodial extensions on the camera lucida reconstruction of the axonal arbor primarily restricted to the stratum lucidum; see also A2. A2, Light micrographs of dendritic spines (top and middle) and of a large MF-like axon varicosity (bottom; arrowheads, main axon; asterisks, filopodia). The asterisk in A1 marks the terminal whose photograph is shown in the bottom panel in A2). A3, Accommodating firing pattern of the cell shown in A1 and A2 in response to depolarizing constant current injection. A4, Accommodating firing pattern of a DG GC. B, CB and Prox1 immunoreactivity of a CA3 GCs (left) and its firing pattern (right). C, CA3 GCs form giant MF terminals in the CA3. Electron micrographs of synaptic contacts formed by the axons of two different CA3 GCs (C1–C3, respectively; C3 is a higher-magnification image of the synaptic contacts in C2). ad, Apical dendrite; b, presynaptic terminal of the labeled CA3 GC; s, postsynaptic spine that originated from the apical dendrite labeled ad. Note the multiple synaptic specializations formed on the same postsynaptic structure (arrowheads), the large number of presynaptic vesicles, and the large size of the terminals, all typical characteristics of giant MF terminals.

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    Figure 3.

    Synaptic outputs of CA3 GCs. A, Monosynaptically connected CA3 GC-to-CA3 PC pair: gray traces, CA3 GC; black traces, CA3 PC. Note the facilitation of the average postsynaptic EPSC (A1) in response to a high-frequency burst of presynaptic action potentials (7 action potentials at 50 Hz) and the short onset delay of the individual responses (A2; illustrated events were in response to the 7th AP from the 50 Hz train). B, Onset delays (from the peak of presynaptic spike to the EPSC onset) for individual monosynaptic (dark bars) and polysynaptic (gray bars) pairs (note that the postsynaptic cells included both CA3 PCs and CA3 GABAergic neurons). Inset, Example traces from a polysynaptic connection between a CA3 GC (gray) and a CA3 PC (black). The calibration bar in A2 also applies to B.

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    Figure 4.

    Monosynaptic output from CA3 GCs onto CA3 GABAergic cells. A1, A2, Dendritic structure (A1) and immunocytochemical characterization (A2) of an SLC that received synaptic connection from a CA3 GC. Note that SLCs project to the medial septum and thus have few, if any, local collaterals. A3, Postsynaptic response in the SLC shown in A1, evoked by a train of 50 action potentials at 50 Hz in the CA3 GCs (gray traces). A4, Individual superimposed presynaptic spikes and postsynaptic responses from A3 indicate the tight temporal coupling between the presynaptic action potential and the postsynaptic response. A5, Average probability of transmission from CA3 GC to SLCs (n = 8) during 50 Hz action potential trains (note that the presynaptic action potential train in A3 is aligned with the x-axis, indicating the action potential number in the train). B, C, Dendritic structure, axonal arborization, and immunocytochemical characterization of a CCK-positive RSBC (B) and of an IvyC (C) in the CA3 area and the monosynaptic EPSCs evoked by pairs of action potentials in presynaptic CA3 GCs (gray traces). Note the large responses in both cell types evoked by the presynaptic CA3 GCs (compare with the small initial responses evoked by CA3 GCs in SLCs). Scale bars, 100 μm.

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    Figure 5.

    Mechanisms of postsynaptic effects of CA3 GCs. A1, A2, Effect of the metabotropic glutamate receptor agonist DCG IV (1 μm) on CA3 GC-evoked responses in an SLC and an IvyC (single traces are shown). A3, Summary data of the DCG IV effect on the probability of monosynaptic responses evoked by CA3 GCs in postsynaptic CA3 GABAergic cells (n = 4). Probability values were normalized to predrug control. B, Representative experiment demonstrating the effect of the AMPA/kainate receptor antagonist NBQX (10 μm) on the monosynaptic responses evoked by a CA3 GC in an SLC neuron in the CA3. s.luc., Stratum lucidum; s.pyr., stratum pyramidale.

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    Figure 6.

    Evidence for entorhinal cortical inputs to CA3 GCs. A, Ten consecutive traces (gray) and the average response (black) in a CA3 GC (reconstruction shown on the right) after the stimulation of presumed entorhinal cortical fibers in the presence of 1 μm DVG IV and 5 μm gabazine. Inset, Relative position of the stimulation electrode (near the fissure; not shown) and the cell body (black dot). Note the facilitation of the EPSCs in response to paired pulses, in agreement with the entorhinal origin of the stimulated fibers. Note also that the dendrites of this particular CA3 GCs did not enter the DG. B, Amplitude of individual evoked responses during the washing in of a low concentration of the AMPA/kainate receptor antagonist NBQX in the perfusing medium. Note the gradual decrease of the evoked EPSC, indicative of monosynaptic connections. C, Perforant pathway-evoked responses in a DG GC (note the similarity to the response of the CA3 GC shown in A).

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    Figure 7.

    Synaptic inputs from local CA3 GABAergic cells to CA3 GCs. A, Dendritic structure, representative axonal arborization, and immunocytochemical characterization of a presynaptic IvyC. Note the NPY-positive, SOM-negative nature of the cell; note also the characteristically dense axonal arbor (s.ori., stratum oriens). B, Postsynaptic responses evoked by the IvyC (A; presynaptic spikes elicited at 0.04 Hz) in a CA3 GC. C, Dendritic structure, representative axonal arborization, and immunocytochemical characterization of a presynaptic MFA. Note the axons in the stratum lucidum and in the dentate hilus (closely overlapping with the termination zones of MFs, hence the name of this GABAergic CA3 cell type; s.gran., stratum granulosum of the DG). Note also the immunopositivity to CCK and the immunonegativity for SOM (both features are characteristics of MFAs). D, Postsynaptic responses evoked by the MFA (C; presynaptic spikes elicited at 10 Hz) in a CA3 GCs.

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    Figure 8.

    Differential endocannabinoid signaling at GABAergic synapses on CA3 GCs and DG GCs. A, Depolarization of the postsynaptic CA3 GCs to 0 mV for 500 ms resulted in strong DSI of the MFA-evoked unitary IPSCs. Right, Example traces before, during, and after the suppression. B, Summary data of the average amplitude of IPSCs (including failures) in MFA-to-CA3 GC pairs (n = 5) during DSI protocol. The IPSC amplitudes were normalized to the average of control amplitude value in each pair. The gray bar indicates the time of the postsynaptic depolarization. C, DSI in MFA–CA3 GC pairs were abolished by the application of the CB1 receptor antagonist AM251 (10 μm; control data correspond the same pairs before drug application). D, Similar depolarizations (0.5 s) in DG GCs did not result in detectable DSI of the responses evoked by the local (intradentate), CCK-positive RSBCs (left); longer (2.5 s) postsynaptic depolarization was able to induce DSI in the same pairs (right). E, Summary data of the average amplitude of IPSCs (including failures) in MFA to CA3 PC pairs (n = 3) during DSI protocol (0.5 s). F, Summary of DSI exhibited by CCK+ inputs to three excitatory cell populations after 0.5 s depolarization of the postsynaptic cells. Gray bars show the averages, and the open circles indicate individual experiments (pairs).

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The Journal of Neuroscience: 30 (24)
Journal of Neuroscience
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16 Jun 2010
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Granule Cells in the CA3 Area
János Szabadics, Csaba Varga, János Brunner, Kang Chen, Ivan Soltesz
Journal of Neuroscience 16 June 2010, 30 (24) 8296-8307; DOI: 10.1523/JNEUROSCI.5602-09.2010

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Granule Cells in the CA3 Area
János Szabadics, Csaba Varga, János Brunner, Kang Chen, Ivan Soltesz
Journal of Neuroscience 16 June 2010, 30 (24) 8296-8307; DOI: 10.1523/JNEUROSCI.5602-09.2010
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