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Articles

NMDA Receptor Dependence of Kindling and Mossy Fiber Sprouting: Evidence that the NMDA Receptor Regulates Patterning of Hippocampal Circuits in the Adult Brain

T. Sutula, J. Koch, G. Golarai, Y. Watanabe and J. O. McNamara
Journal of Neuroscience 15 November 1996, 16 (22) 7398-7406; DOI: https://doi.org/10.1523/JNEUROSCI.16-22-07398.1996
T. Sutula
1Departments of Neurology and Anatomy, and the
2Neuroscience Training Program, University of Wisconsin, Madison, Wisconsin 53292, and Departments of
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J. Koch
1Departments of Neurology and Anatomy, and the
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G. Golarai
1Departments of Neurology and Anatomy, and the
2Neuroscience Training Program, University of Wisconsin, Madison, Wisconsin 53292, and Departments of
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Y. Watanabe
3Medicine (Neurology) and
4Neurobiology and Pharmacology, and
5the Epilepsy Research Laboratory, Veterans Affairs Medical Center, Duke University, Durham, North Carolina 27705
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J. O. McNamara
3Medicine (Neurology) and
4Neurobiology and Pharmacology, and
5the Epilepsy Research Laboratory, Veterans Affairs Medical Center, Duke University, Durham, North Carolina 27705
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  • Fig. 1.
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    Fig. 1.

    Horizontal section of the hippocampus and DG in a normal rat stained by the Timm method demonstrates the normal terminal field of the mossy fiber axons arising from granule cells in the DG. Dense areas of dark staining areas in the DG and CA3 fields are locations of synapses of mossy fiber axons, which stain darkly because of their high content of Zn. The area outlined by thebox is the standard location in the DG that was evaluated by scoring methods for Timm histochemistry. H, Hilus; DG, dentate gyrus. Scale bar, 1000 μm.

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    Fig. 2.

    Examples of continuous recordings from a depth electrode in the perforant path of rats that received injections of either saline (A) saline or MK801 (B) 30 min before stimulation of the perforant path with a 1 sec train of 62 Hz, 1 msec biphasic constant current pulses (arrowhead). A, In a saline-injected rat, a perforant path stimulus of 500 μA evoked an AD that began with a brief run of high-frequency spike discharges that was immediately followed by repetitive irregular spike and spike-wave discharges that gradually decreased in frequency, which were followed by lower-amplitude featureless activity. The arrowindicates the end of the AD, which had a duration of 43 sec.B, In a rat treated with MK801 30 min before perforant path stimulation, a 1400 μA stimulus train evoked an AD that also began with brief high-frequency discharges that evolved into repetitive spike and irregular spike-wave discharges. The arrow at the onset of low-amplitude featureless activity indicates the end of the AD, which had a duration of 64 sec. Calibration bars are for bothA and B. Rats pretreated with MK801 had a higher initial AD threshold and experienced ADs of longer duration than saline-injected controls (see text and Table 2 for details).

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    Fig. 3.

    Higher-magnification views of horizontal Timm-stained sections in the standard location in the DG described in Figure 1. A, Higher magnification of the boxed area in Figure 1 demonstrates the appearance of the supragranular area of the DG from a normal rat, which is not innervated by mossy fiber axons and has few or no dark staining granules (open arrows). B, Higher magnification of the same region in a kindled rat that received once-daily stimulation that evoked 14 afterdischarges and 1 class V secondary generalized tonic–clonic seizure. The supragranular region contains numerous dark Timm granules corresponding to synapses of mossy fiber axons, which form a laminar band (filled arrows).C, Higher magnification from the same region in a rat that received MK801 before each stimulation until 17 afterdischarges were evoked. Timm granules are present in the supragranular layer (filled arrows) but are not as prominent as in the untreated rat in B. D, Higher magnification from the same region in a rat that received MK801 before each stimulation beginning after the 10th afterdischarge and continuing until 1 class V seizure was evoked. The supragranular region contains numerous dark Timm granules that form a laminar band (filled arrows). Untreated rats that experienced 1 class V seizure had comparable mossy fiber synaptic reorganization, as assessed by Timm scores (see Table 2). H, Hilus. Scale bar (shown in A): 100 μm.

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    Fig. 4.

    A, Higher magnification of the DG in a kindled rat that received once-daily stimulation that evoked 25 afterdischarges and 10 class V secondary generalized tonic–clonic seizures. The supragranular region contains numerous dark Timm granules corresponding to synapses of mossy fiber axons, which form a laminar band (filled arrows).B, Higher magnification from the same region in a rat that received MK801 before each stimulation after the first class V seizure and continuing until 10 class V seizures were evoked. This rat required 34 afterdischarges to evoke 10 class V seizures. The supragranular region also contains a laminar band of Timm granules (filled arrows). H, Hilus. Scale bar (shown in A): 100 μm.

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    Fig. 5.

    Summary of the effects of MK801 on the kindling rate and mossy fiber synaptic reorganization for groups of control rats and rats treated with MK801. The kindling rate was expressed as the mean number of afterdischarges, and mossy fiber synaptic reorganization was assessed by mean Timm scores. The error bars indicate the SEM for each group; *, versus Timm score for CONTROL 1 CL V, p = 0.032; **, versus kindling rate forCONTROL 1 CL V, p = 0.012; ***, versus kindling rate for CONTROL 10 Cl V, p = 0.024.

Tables

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    Table 1.

    Effects of MK801 and kindling on afterdischarge threshold (microamps ± SEM)

    1st AD1_15010th AD11th AD17th AD1st class V2nd class V10th class V
    Controls561  ± 42495  ± 39491  ± 40467  ± 79467  ± 47−−
    1 class V
    Controls562  ± 73490  ± 60484  ± 61437  ± 61435  ± 55417  ± 57314  ± 52
    10 class V
    MK8011007  ± 1331_151900  ± 102885  ± 106785  ± 100−−−
    0–17 ADs
    MK801572  ± 49517  ± 44505  ± 49439  ± 42364  ± 35−−
    10 ADs–1 class V
    MK801594  ± 53575  ± 67566  ± 66455  ± 43471  ± 49453  ± 44282  ± 33
    1–10 class V
    • ↵F1_150 Versus final AD thresholds, F = 16.4, p = 0.0001, ANOVA;

    • ↵F1_151 versus initial AD thresholds, F = 6.5, p = 0.0004, ANOVA.

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    Table 2.

    MK801 pretreatment versus controls

    Experimental groupAD2_150Cumulative AD duration (sec)2_150Timm score2_150
    Normal control (n = 7)−−0.8  ± 0.13
    Kindling17.2  ± 1.8624  ± 543.44  ± 0.29
    1 Cl V
    (n = 9)
    MK80117840  ± 582_a2.43  ± 0.322_b
    0–17 ADs
    (n = 7)
    MK80124.2  ± 1.71166  ± 1102_c3.39  ± 0.22
    10 AD–1 Cl V
    (n = 9)
    Kindling29.3  ± 1.61451  ± 833.54  ± 0.3
    10 Cl V
    (n = 8)
    MK80135.7  ± 1.92066  ± 482_d3.29  ± 0.27
    1–10 Cl V
    (n = 9)
    • ↵F2_150 p < 0.0001, ANOVA.

    • ↵F2_a  versus kindling 1 Cl V, p < 0.017.

    • ↵F2_b  versus kindling 1 Cl V, p < 0.032.

    • ↵F2_c  versus kindling 1 Cl V, p < 0.001.

    • ↵F2_d  versus kindling 10 Cl V, p < 0.00001.

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The Journal of Neuroscience: 16 (22)
Journal of Neuroscience
Vol. 16, Issue 22
15 Nov 1996
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NMDA Receptor Dependence of Kindling and Mossy Fiber Sprouting: Evidence that the NMDA Receptor Regulates Patterning of Hippocampal Circuits in the Adult Brain
T. Sutula, J. Koch, G. Golarai, Y. Watanabe, J. O. McNamara
Journal of Neuroscience 15 November 1996, 16 (22) 7398-7406; DOI: 10.1523/JNEUROSCI.16-22-07398.1996

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NMDA Receptor Dependence of Kindling and Mossy Fiber Sprouting: Evidence that the NMDA Receptor Regulates Patterning of Hippocampal Circuits in the Adult Brain
T. Sutula, J. Koch, G. Golarai, Y. Watanabe, J. O. McNamara
Journal of Neuroscience 15 November 1996, 16 (22) 7398-7406; DOI: 10.1523/JNEUROSCI.16-22-07398.1996
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Keywords

  • NMDA
  • kindling
  • sprouting
  • hippocampus
  • plasticity
  • receptors
  • MK801
  • dentate gyrus
  • seizures epilepsy

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