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Research ArticleNew Research, Cognition and Behavior

Noninvasive Brain Stimulation Enhances Memory Acquisition and Is Associated with Synaptoneurosome Modification in the Rat Hippocampus

Seung Ho Jung, Candice Hatcher-Solis, Raquel Moore, Naomi Bechmann, Sean Harshman, Jennifer Martin and Ryan Jankord
eNeuro 7 November 2019, 6 (6) ENEURO.0311-19.2019; DOI: https://doi.org/10.1523/ENEURO.0311-19.2019
Seung Ho Jung
1Applied Neuroscience Branch, 711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson AFB, OH 45433
2Research Associateship Program, National Research Council, National Academies of Science, Washington, DC 200001
3ORISE, Oak Ridge, TN 37830
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Candice Hatcher-Solis
1Applied Neuroscience Branch, 711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson AFB, OH 45433
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  • ORCID record for Candice Hatcher-Solis
Raquel Moore
1Applied Neuroscience Branch, 711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson AFB, OH 45433
4Infoscitex, Dayton, OH 45431
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Naomi Bechmann
1Applied Neuroscience Branch, 711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson AFB, OH 45433
4Infoscitex, Dayton, OH 45431
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Sean Harshman
5UES, Inc, Dayton, OH 45432
6Human Signatures Branch, 711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson AFB, OH 45433
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Jennifer Martin
6Human Signatures Branch, 711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson AFB, OH 45433
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Ryan Jankord
1Applied Neuroscience Branch, 711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson AFB, OH 45433
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Figures

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  • Figure 1.
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    Figure 1.

    Overall research design. *Before rodents were exposed to the passive avoidance memory task, they were freely exposed to open field for 5 min (the acquisition day) and 3 min (the training and testing days) for exploration with familiar and novel objects similar to the novel object recognition task. Proteomic abundance data were first analyzed for the replicability within each group (Extended Data Fig. 1-1), and the abundance of 16 internal control proteins was compared between the groups (Extended Data Fig. 1-2). Proteomic data analyzed for this manuscript were provided as an Excel file (Extended Data Fig. 1-3).

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    Figure 2.

    Behavioral data analysis. A, Analysis of passive avoidance data. Two-way RM ANOVA detected a significant difference in the latency of all groups between the training and testing days. During the testing day, a statistical significance was detected between sham and acquisition groups. #Habituation data were collected from only eight animals per group; * and ** indicate statistical significance (p < 0.05 and p < 0.001, respectively). B, Cox proportional hazard regression analysis for PAT data on training day. No statistical group separation was detected. C, Cox proportional hazard regression analysis for PAT data on testing day. A significant group difference was detected (log-rank Χ 2 = 7.0919, df = 2, p = 0.0288). D, PCA with proteomics data show the distribution of each samples across the groups. E, Hierarchical clustering analysis with proteomics data show the distribution of each sample across the groups. Red, green, and blue boxes represent sham, retrieval, and acquisition samples. Protein IDs in the first hierarchical clustering group, from left to right, are KDELC2, EXOC6, UFL1, CDH8, ARHGAP27, BLNK, MPPED2, GFM1, FNTB, WASH, PDE4DIP, TUBA4A, ACVR1B, PRKAR1B, RBMX2, ZFYVE27, CAPN5, PSME1, KCNA6, LLGL1, JAM3, CD151, S1PR5, and GPSM1. The hierarchical clustering group 2 includes, from left to right, LHX1, GUCY1A2, STX8, CSAD, USP19, FTSJD2, DNAH7, LOC362863, RAB9A, GSTZ1, PDIA4, RPH3AL, LRFN1, STK39, CCDC116, LOC100911646, GLS, PYROXD2, LOC100911456, AOC3, MYO1C, and ILK. For the cluster group 3, protein IDs are INHBA, EIF3J, SLC20A1, ZRANB2, CCDC127, FAM195B, GLDN, FHIT, PNPO, PGP, TUBA1C, ACBD6, MCCC1, NOP58, ITGAD, RPL27, ABCF1, WDR81, and COTL1. The cluster group 4 contains proteins named as, from left to right, CACNA1D, GHITM2, SCFD1, PTP4A2, ZW10, GCLM, APMAP, CRP, SRP54, PTPRN2, SRP542, ADCY6, CAR3, COL3A1, IP6K1, GOLPH31, SLC27A1, RILPL1, PFKFB1, PSMA2, and ICOS. Proteins from the cluster group 5 are GALE, EQTN, CLUL1, GABRB2, MRPS25, MRAS, SCYL1, OXCT1, FAM194A, FAM213B, LAMP5, SNX1, CNIH2, GHITM, SLC29A3, and AK6. Proteins in the cluster group 6 are MARK2, HOMER3, GPHN, RAB3GAP2, RBP1, PALMD, MCCC2, ARHGEF11, and LRRC57. For a clear figure, see Extended Data Figure 2-1.

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    Figure 3.

    IPA results. A, Behavior-associated functional annotation detected from the comparison between the acquisition and sham groups. B, Network-1 detected from the comparison between the retrieval and sham groups. C, Six networks that were associated with the nervous system were merged in to a network. Nodes that did not pass cutoff in dataset, not in overlaid dataset, and not connected to any other nodes were excluded from the network. Pink-outlined molecules are associated with cognition (p = 1.81E-3). Molecule activity predictor (MAP) was also overlaid to predict the upstream and downstream effects of activation or inhibition on other molecules. For all IPA data, see Extended Data Figures 3-1, 3-2, 3-3, 3-4.

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    Figure 4.

    PPI network analysis. A, PPI network for the significant molecules from the acquisition-and-sham comparison. Nodes were colored for functions of glutamatergic synapse (blue), metabolic pathways (yellow), dopaminergic synapse (green), LTP (red), and cholinergic synapse (pink). Disconnected nodes were excluded. B, The first cluster network of MCL algorithm. C, The second cluster network of MCL algorithm.

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    Figure 5.

    PSS network analysis. The BLASTP suite (BLASTP 2.8.0+) was used to search proteins and determine their sequence similarity. PSS network was created by using Cytoscape. The PSS network was clustered by using ClusterONE, and nine clusters were significantly identified. The edges were weighted by their sequence similarity and the enrichment analysis was performed for each of the nine clusters to identify specific signaling pathways of the clusters.

Tables

  • Figures
  • Extended Data
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    Table 1.

    Results of PantherDB analysis for the comparison between sham and acquisition groups

    PANTHER GO-Slim pathwaysOver/UnderFold enrichmentRaw
    p value
    FDR
    (q value)
    Cellular ComponentPostsynaptic membrane (GO:0045211)+30.259.68E-113.10E-09
    Neuromuscular junction (GO:0031594)+25.213.67E-042.14E-03
    Synapse (GO:0045202)+12.672.09E-111.34E-09
    Dendrite (GO:0030425)+9.717.15E-079.15E-06
    Neuron projection (GO:0043005)+7.038.27E-091.77E-07
    Cell junction (GO:0030054)+6.923.10E-041.98E-03
    Cell projection (GO:0042995)+4.93.05E-074.88E-06
    Integral to membrane (GO:0016021)+2.693.03E-052.42E-04
    Plasma membrane (GO:0005886)+2.434.05E-063.70E-05
    Cytoskeleton (GO:0005856)+2.319.41E-034.63E-02
    Membrane (GO:0016020)+2.143.70E-063.94E-05
    Protein complex (GO:0043234)+2.10.00017.14E-04
    Biological ProcessGrowth (GO:0040007)+44.129.25E-052.51E-03
    Asymmetric protein localization (GO:0008105)+35.291.58E-043.86E-03
    Muscle organ development (GO:0007517)+26.143.03E-071.85E-05
    Neuron-neuron synaptic transmission (GO:0007270)+13.071.27E-081.55E-06
    Pyrimidine nucleobase metabolic process (GO:0006206)+11.392.91E-033.55E-02
    Synaptic transmission (GO:0007268)+6.384.01E-119.80E-09
    Ion transport (GO:0006811)+4.482.13E-068.66E-05
    Cell-cell signaling (GO:0007267)+4.432.12E-081.72E-06
    Cytoskeleton organization (GO:0007010)+3.221.35E-032.20E-02
    Protein localization (GO:0008104)+2.881.20E-032.08E-02
    Transport (GO:0006810)+2.354.58E-061.60E-04
    Localization (GO:0051179)+2.349.21E-074.50E-05
    Neurological system process (GO:0050877)+2.113.25E-047.21E-03
    System process (GO:0003008)+2.054.42E-048.30E-03
    Phosphate-containing compound metabolic process (GO:0006796)+1.941.45E-032.09E-02
    Cellular component organization (GO:0016043)+1.762.71E-033.48E-02
    Cell communication (GO:0007154)+1.553.25E-033.77E-02
    Sensory perception of smell (GO:0007608)-<0.012.15E-032.92E-02
    Sensory perception of chemical stimulus (GO:0007606)-<0.011.44E-032.19E-02
    Sensory perception (GO:0007600)-<0.010.0004260.00866
    Molecular FunctionGlutamate receptor activity (GO:0008066)+22.967.33E-093.50E-07
    Nucleotide kinase activity (GO:0019201)+20.171.16E-063.70E-05
    Voltage-gated calcium channel activity (GO:0005245)+13.072.02E-033.51E-02
    Ligand-gated ion channel activity (GO:0015276)+9.83.71E-081.42E-06
    Voltage-gated ion channel activity (GO:0005244)+8.111.37E-042.91E-03
    Voltage-gated potassium channel activity (GO:0005249)+7.592.34E-033.44E-02
    Ion channel activity (GO:0005216)+7.131.86E-113.56E-09
    Cation channel activity (GO:0005261)+5.123.51E-034.19E-02
    Small GTPase regulator activity (GO:0005083)+4.642.25E-033.59E-02
    Transmembrane transporter activity (GO:0022857)+3.84.03E-093.84E-07
    Transporter activity (GO:0005215)+3.544.84E-093.08E-07
    GTPase activity (GO:0003924)+3.131.67E-033.19E-02
    Kinase activity (GO:0016301)+2.522.41E-033.29E-02
    Pyrophosphatase activity (GO:0016462)+2.383.84E-034.31E-02
    Catalytic activity (GO:0003824)+1.743.98E-061.08E-04
    Protein binding (GO:0005515)+1.640.003130.0399
    • * See Extended Data Table 1-1 for all Reactome pathway terms identified from the comparison between sham and acquisition groups.

    • View popup
    Table 2.

    Results of PantherDB analysis for the comparison between sham and retrieval groups

    PANTHER GO-Slim pathwaysOver/UnderFold enrichmentRaw
    p value
    FDR
    (q value)
    Cellular ComponentPostsynaptic membrane (GO:0045211)+14.719.98E-097.99E-08
    Neuromuscular junction (GO:0031594)+11.033.83E-031.29E-02
    Proton-transporting ATP synthase complex (GO:0045259)+9.81.20E-034.51E-03
    Synapse (GO:0045202)+8.311.24E-127.96E-11
    Mitochondrial inner membrane (GO:0005743)+7.14.77E-095.08E-08
    Dendrite (GO:0030425)+7.081.49E-081.06E-07
    SNARE complex (GO:0031201)+6.065.75E-031.84E-02
    Neuron projection (GO:0043005)+5.332.61E-115.57E-10
    Cell junction (GO:0030054)+5.055.70E-052.60E-04
    Axon (GO:0030424)+4.681.31E-023.98E-02
    Cell projection (GO:0042995)+3.757.41E-096.77E-08
    Protein complex (GO:0043234)+2.318.91E-122.85E-10
    Cytoskeleton (GO:0005856)+2.25.35E-042.14E-03
    Membrane (GO:0016020)+1.991.14E-091.46E-08
    Integral to membrane (GO:0016021)+1.875.15E-042.20E-03
    Macromolecular complex (GO:0032991)+1.792.02E-071.17E-06
    Cytoplasm (GO:0005737)+1.765.38E-108.61E-09
    Plasma membrane (GO:0005886)+1.591.62E-035.77E-03
    Cell part (GO:0044464)+1.441.96E-071.25E-06
    Intracellular (GO:0005622)+1.372.18E-051.07E-04
    Biological Process*Growth (GO:0040007)+19.31.01E-038.82E-03
    Asymmetric protein localization (GO:0008105)+15.441.70E-031.34E-02
    Oxidative phosphorylation (GO:0006119)+10.892.67E-089.31E-07
    Pyrimidine nucleobase metabolic process (GO:0006206)+8.35.69E-046.31E-03
    JNK cascade (GO:0007254)+8.046.47E-046.32E-03
    Respiratory electron transport chain (GO:0022904)+7.353.03E-091.48E-07
    Generation of precursor metabolites and energy (GO:0006091)+6.031.52E-113.72E-09
    Neuron-neuron synaptic transmission (GO:0007270)+5.722.13E-053.25E-04
    Purine nucleobase metabolic process (GO:0006144)+5.634.04E-044.93E-03
    Glycolysis (GO:0006096)+5.511.15E-039.39E-03
    Mitochondrial transport (GO:0006839)+5.483.06E-031.86E-02
    Neurotransmitter secretion (GO:0007269)+4.981.46E-041.98E-03
    Cation transport (GO:0006812)+4.241.89E-031.44E-02
    Calcium-mediated signaling (GO:0019722)+4.142.14E-031.45E-02
    Mitochondrion organization (GO:0007005)+42.56E-031.65E-02
    Synaptic transmission (GO:0007268)+3.995.54E-104.51E-08
    Anatomical structure morphogenesis (GO:0009653)+3.686.22E-046.60E-03
    Protein targeting (GO:0006605)+3.475.29E-046.15E-03
    Ion transport (GO:0006811)+2.871.82E-052.96E-04
    Cell-cell signaling (GO:0007267)+2.863.92E-079.58E-06
    Molecular Function*Glutamate receptor activity (GO:0008066)+11.33.82E-079.12E-06
    Nucleotide kinase activity (GO:0019201)+10.291.32E-051.94E-04
    SNAP receptor activity (GO:0005484)+7.353.07E-032.66E-02
    Hydrogen ion transmembrane transporter activity (GO:0015078)+7.054.00E-068.48E-05
    Carbohydrate kinase activity (GO:0019200)+6.644.27E-033.26E-02
    Anion channel activity (GO:0005253)+5.253.61E-032.87E-02
    Ligand-gated ion channel activity (GO:0015276)+5.074.31E-068.24E-05
    Voltage-gated ion channel activity (GO:0005244)+4.142.14E-032.27E-02
    Ion channel activity (GO:0005216)+4.065.90E-093.76E-07
    Cation channel activity (GO:0005261)+3.582.49E-032.51E-02
    Microtubule binding (GO:0008017)+3.45.95E-034.37E-02
    Small GTPase regulator activity (GO:0005083)+3.391.12E-031.34E-02
    Oxidoreductase activity (GO:0016491)+35.89E-081.88E-06
    Kinase activity (GO:0016301)+2.792.71E-077.39E-06
    Calcium ion binding (GO:0005509)+2.792.80E-032.54E-02
    • ↵* See Extended Data Table 2-1 for all GO-Slim pathway terms.

    • View popup
    Table 3.

    Results of DAVID Bioinformatics analysis for the comparison between sham and acquisition groups

    Functional annotation term summary*Enrichment scoreFDR (q value)
    ClusterMedian SDLowestHighest
    1Postsynaptic membrane13.965.88E-130.0551.65E-200.18
    2Synapse12.406.63E-120.0411.65E-200.092
    3Ion transport9.543.25E-074.75E-071.49E-071.05E-06
    4Mitochondrial inner membrane7.440.01540.0932.25E-120.19
    5Positive regulation of excitatory postsynaptic potential5.230.00140.8483.79E-041.47
    6Neuronal membrane-associated guanylate kinases5.160.01630.2244.25E-040.46
    7PDZ and SH3 domains4.910.012119.781.44E-0765.75
    8Ionotropic glutamate and NMDA receptors4.860.02720.8593.01E-041.50
    9AMPA glutamate receptor complex4.420.01045.280.00189.15
    10Glutamatergic synapses4.340.163625.261.44E-07100.0
    11Guanylate-kinase-associated protein4.251.08430.6824.25E-041.26
    • ↵* See Extended Data Table 3-1 for detailed functional clustering annotation terms.

Extended Data

  • Figures
  • Tables
  • Extended Data Figure 1-1

    Replicability of proteomic abundance data within each group. The abundance values within each group were analyzed and the lowest r2 for the sham, acquisition and retrieval groups were 0.89, 0.91, and 0.72, respectively. Download Figure 1-1, TIF file.

  • Extended Data Figure 1-2

    Abundance comparison of 16 internal control proteins between groups. None of all 16 internal control proteins resulted in no significant difference between acquisition and sham groups. The comparison between retrieval and sham groups, one internal control protein (Aldoa) showed a significant group difference. The abundance data of three internal control proteins (Aldoa, Gdir1, and Pgk1) resulted in a significant group difference between acquisition and retrieval groups. Download Figure 1-2, TIF file.

  • Extended Data Figure 1-3

    Proteomics data. Proteomics data analyzed for this manuscript were provided as an Excel file. Download Figure 1-3, XLSX file.

  • Extended Data Figure 2-1

    Hierarchical clustering analysis with proteomics data show the distribution of each sample across the groups. Download Figure 2-1, TIF file.

  • Extended Data Table 1-1

    Results of Reactome pathway analysis for the comparison between sham and acquisition groups Download Table 1-1, XLSX file.

  • Extended Data Table 2-1

    Results of GO slim analysis for the comparison between acquisition and retrieval groups Download Table 2-1, XLSX file.

  • Extended Data Table 3-1

    Results of functional clustering annotation analysis for the comparison between sham and acquisition groups. Download Table 3-1, XLSX file.

  • Extended Data Figure 3-1

    IPA diseases or functions annotation for the comparison between retrieval and sham groups. Download Figure 3-1, XLSX file.

  • Extended Data Figure 3-2

    IPA diseases or functions annotation for the comparison between acquisition and sham groups Download Figure 3-2, XLSX file.

  • Extended Data Figure 3-3

    Lists of IPA-generated networks for the comparisons between retrieval and sham groups and between acquisition and sham groups Download Figure 3-3, XLSX file.

  • Extended Data Figure 3-4

    Top regulators from the IPA upstream analysis for the comparisons between retrieval and sham groups and between acquisition and sham groups. Download Figure 3-4, XLSX file.

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Noninvasive Brain Stimulation Enhances Memory Acquisition and Is Associated with Synaptoneurosome Modification in the Rat Hippocampus
Seung Ho Jung, Candice Hatcher-Solis, Raquel Moore, Naomi Bechmann, Sean Harshman, Jennifer Martin, Ryan Jankord
eNeuro 7 November 2019, 6 (6) ENEURO.0311-19.2019; DOI: 10.1523/ENEURO.0311-19.2019

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Noninvasive Brain Stimulation Enhances Memory Acquisition and Is Associated with Synaptoneurosome Modification in the Rat Hippocampus
Seung Ho Jung, Candice Hatcher-Solis, Raquel Moore, Naomi Bechmann, Sean Harshman, Jennifer Martin, Ryan Jankord
eNeuro 7 November 2019, 6 (6) ENEURO.0311-19.2019; DOI: 10.1523/ENEURO.0311-19.2019
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Keywords

  • hippocampal proteomics
  • hippocampal synaptoneurosome
  • memory process
  • protein sequence similarity network
  • protein-protein interaction network
  • transcranial direct current stimulation

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