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Research Articles, Systems/Circuits

Dopaminergic Modulation of Synaptic Integration and Firing Patterns in the Rat Entopeduncular Nucleus

Hagar Lavian, Mara Almog, Ravit Madar, Yocheved Loewenstern, Izhar Bar-Gad, Eitan Okun and Alon Korngreen
Journal of Neuroscience 26 July 2017, 37 (30) 7177-7187; DOI: https://doi.org/10.1523/JNEUROSCI.0639-17.2017
Hagar Lavian
1The Leslie and Susan Gonda Interdisciplinary Brain Research Center,
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Mara Almog
2The Mina and Everard Goodman Faculty of Life Sciences, and
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Ravit Madar
1The Leslie and Susan Gonda Interdisciplinary Brain Research Center,
2The Mina and Everard Goodman Faculty of Life Sciences, and
3The Paul Feder Laboratory on Alzheimer's disease research, Bar Ilan University, Ramat Gan 52900, Israel
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Yocheved Loewenstern
1The Leslie and Susan Gonda Interdisciplinary Brain Research Center,
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Izhar Bar-Gad
1The Leslie and Susan Gonda Interdisciplinary Brain Research Center,
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Eitan Okun
1The Leslie and Susan Gonda Interdisciplinary Brain Research Center,
2The Mina and Everard Goodman Faculty of Life Sciences, and
3The Paul Feder Laboratory on Alzheimer's disease research, Bar Ilan University, Ramat Gan 52900, Israel
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Alon Korngreen
1The Leslie and Susan Gonda Interdisciplinary Brain Research Center,
2The Mina and Everard Goodman Faculty of Life Sciences, and
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  • Figure 1.
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    Figure 1.

    Postsynaptic expression of dopamine receptors in the EP. A, Expression levels of dopamine receptor mRNA in the EP, obtained with qRT-PCR (n = 5). Expression levels, expressed as the mean ± SEM, were normalized to the expression levels of D1R. B, Expression levels of dopamine receptor mRNA in the striatum, obtained with qRT-PCR (n = 5). Inset shows enlarged data for DR3 to DR5.

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    Figure 2.

    Striatum–EP IPSCs are modulated by D1LR receptors, but not D2LR receptors. A, D, Whole-cell voltage-clamp recordings of striatum evoked IPSCs in control conditions (black) and after the application of SCH23390 (A, red) or sulpiride (D, blue) averaged over 10 consecutive sweeps. B, E, Population average of striatum-evoked IPSCs in control conditions and after the application of SCH23390 (B, n = 8) or sulpiride (E, n = 5). C, F, The amplitude of the first evoked IPSC in the controls and after the application of SCH23390 (C) or sulpiride (F). Values are given as the mean ± SEM. *p < 0.05, **p < 0.01.

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    Figure 3.

    GP–EP IPSCs are modulated by D2LR receptors, but not D1LR receptors. A, D, Whole-cell voltage-clamp recordings of GP-evoked IPSCs in control conditions (black) and after application of SCH23390 (A, red) or sulpiride (D, blue) averaged over 10 consecutive sweeps. B, E, Population average of GP-evoked IPSCs in control conditions and after the application of SCH23390 (B, n = 7) or sulpiride (E, n = 19). C, F, The amplitude of the first evoked IPSC in the controls and after application of SCH23390 (C) or sulpiride (F). Values are given as the mean ± SEM. *p < 0.05, **p < 0.01.

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    Figure 4.

    Striatal inputs induce a continuous decrease in spike time entropy of EP neurons in a dopamine-dependent manner. A, Effects of repetitive activation of striatal synapses on the firing pattern in the EP. Repetitive stimulation of the striatum at 20 Hz, where arrows indicate the timing of stimulation pulses. In this and all subsequent recordings, stimulation artifacts were removed for clarity. Ten sweeps were overlaid to more clearly show the effect of the stimulations. Bi, Bii, Raster plots of the response of an EP neuron to 20 Hz stimulation of the striatum in control conditions (Bi) and after application of SCH23390 (Bii). Ci, Cii, Changes in firings rate induced by 20 Hz stimulation of the striatum in control conditions (Ci) and after application of SCH23390 (Cii; n = 9). Ciii, Normalized firing rate at the time of the last IPSC evoked by 10 or 20 Hz stimulation in the controls and after application of SCH23390. Di, Dii, changes in spike time entropy induced by 20 Hz stimulation of the striatum in the control conditions (Di) and after application of SCH23390 (Dii; n = 9). Diii, Normalized entropy at the time of the last evoked IPSC in the controls and after application of SCH23390. Ei, Eii, Changes in the SD of the latency of spike discharge induced by each evoked IPSP calculated for 20 Hz stimulation of the striatum in control conditions (Ei) and after the application of SCH23390 (Eii; n = 6). Eiii, Normalized change in the SD of the latency at the time of the last evoked IPSC in control and after application of SCH23390. Values are given as the mean ± SEM. **p < 0.001, *p < 0.05.

  • Figure 5.
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    Figure 5.

    GP inputs induce a transient decrease in spike time entropy of EP neurons in a dopamine-dependent manner. A, Repetitive stimulation of the GP at 20 Hz, arrows indicate timing of stimulation pulses. Ten sweeps were overlaid to more clearly show the effect of the stimulations on the spontaneous activity. Bi, Bii, Raster plots of the response of an EP neuron to 20 Hz stimulation of the GP in control conditions (Bi) and after application of sulpiride (Bii). Ci, Cii, Changes in firings rate induced by 20 Hz stimulation of the GP in control conditions (Ci) and after application of sulpiride (Cii; n = 5). Ciii, Normalized firing rate at the time of the first evoked IPSC in control and after application of sulpiride. Di, Dii, Changes in spike time entropy induced by 20 Hz stimulation of the GP in control conditions (Di) and after application of sulpiride (Dii; n = 5). Diii, Normalized entropy at the time of the first evoked IPSC in control and after application of sulpiride. Ei, Eii, Changes in the SD of the latency of spike discharge induced by each evoked IPSP calculated for 20 Hz stimulation of the GP in control conditions (Ei) and after application of sulpiride (Eii; n = 6). Values are given as the mean ± SEM. *p < 0.05.

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    Figure 6.

    Simulated data show that striatum and GP inputs can modulate the firing of Poisson neurons. A, E, Raster plots of the response of a simulated Poisson neuron to 20 Hz stimulation of the striatum (A) and the GP (E). B, F, Changes in spike time entropy induced by 20 Hz stimulation of the striatum (B) and the GP (F; n = 10). C, G, Changes in average latency of spike discharge induced by each evoked IPSP calculated for 20 Hz stimulation of the striatum (C) and the GP (G; n = 10). D, H, Changes in the SD of the latency of spike discharge induced by each evoked IPSP calculated for 20 Hz stimulation of the striatum (D) and the GP (H; n = 10). In all panels, the experimental data are presented with black symbols and LIF stimulation is presented with red symbols. The results of the simulation were not fitted to the data; they were overlaid on the experiments to allow for qualitative comparison. Values are given as the mean ± SEM.

Tables

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    Table 1.

    Primers used for quantitative real-time PCR to assess mRNA expression of the five subtypes of dopamine receptors and β-actin

    GeneAnnealing temperatureAccession numberProduct length (bp)Primer sequences
    DRD155°CNM_012546.3168Forward: 5′-TCCTTCAAGAGGGAGACGAA-3′
    Reverse: 5′-CCACACAAACACATCGAAGG-3′
    DRD258°CNM_012547.1230Forward: 5′-CATTGTCTGGGTCCTGTCCT-3′
    Reverse: 5′-GCTCTGAAAGCTCGACTGCT-3′
    DRD359°CNM_017140.2104Forward: 5′-GAGCTCCTGTAGACGTGTGG-3′
    Reverse: 5′-TGGGATCCCCTGTTGTGTTG-3′
    DRD456°CNM_012944.2166Forward: 5′-GTAGTTGGGGCCTTCCTGTA-3′
    Reverse: 5′-CGGCATTGAAGATGGTGTAG-3′
    DRD558°CNM_012768.1146Forward: 5′-GTATCATCAGCGTGGACCGT-3′
    Reverse: 5′-CCAATTGAGTTGGACCGGGA-3′
    Actin56°CNM_031144.3165Forward: 5′-TGTCACCAACTGGGACGATA-3′
    Reverse: 5′-GGGGTGTTGAAGGTCTCAAA-3′
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The Journal of Neuroscience: 37 (30)
Journal of Neuroscience
Vol. 37, Issue 30
26 Jul 2017
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Dopaminergic Modulation of Synaptic Integration and Firing Patterns in the Rat Entopeduncular Nucleus
Hagar Lavian, Mara Almog, Ravit Madar, Yocheved Loewenstern, Izhar Bar-Gad, Eitan Okun, Alon Korngreen
Journal of Neuroscience 26 July 2017, 37 (30) 7177-7187; DOI: 10.1523/JNEUROSCI.0639-17.2017

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Dopaminergic Modulation of Synaptic Integration and Firing Patterns in the Rat Entopeduncular Nucleus
Hagar Lavian, Mara Almog, Ravit Madar, Yocheved Loewenstern, Izhar Bar-Gad, Eitan Okun, Alon Korngreen
Journal of Neuroscience 26 July 2017, 37 (30) 7177-7187; DOI: 10.1523/JNEUROSCI.0639-17.2017
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Keywords

  • basal ganglia
  • dopamine
  • entopeduncular
  • entropy
  • GABA
  • patch clamp
  • plasticity

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