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Research ArticleResearch Article: New Research, Cognition and Behavior

Exploring the Role of the Nucleus Accumbens in Adaptive Behavior Using Concurrent Intracranial and Extracranial Electrophysiological Recordings in Humans

Nadine Eijsker, Guido van Wingen, Ruud Smolders, Dirk J. A. Smit and Damiaan Denys
eNeuro 9 November 2020, 7 (6) ENEURO.0105-20.2020; https://doi.org/10.1523/ENEURO.0105-20.2020
Nadine Eijsker
1Department of Psychiatry, Amsterdam Neuroscience, Amsterdam UMC, University of Amsterdam, Amsterdam, 1105 AZ, The Netherlands
2Amsterdam Brain and Cognition, University of Amsterdam, Amsterdam, 1001 NK, The Netherlands
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  • ORCID record for Nadine Eijsker
Guido van Wingen
1Department of Psychiatry, Amsterdam Neuroscience, Amsterdam UMC, University of Amsterdam, Amsterdam, 1105 AZ, The Netherlands
2Amsterdam Brain and Cognition, University of Amsterdam, Amsterdam, 1001 NK, The Netherlands
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Ruud Smolders
1Department of Psychiatry, Amsterdam Neuroscience, Amsterdam UMC, University of Amsterdam, Amsterdam, 1105 AZ, The Netherlands
2Amsterdam Brain and Cognition, University of Amsterdam, Amsterdam, 1001 NK, The Netherlands
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Dirk J. A. Smit
1Department of Psychiatry, Amsterdam Neuroscience, Amsterdam UMC, University of Amsterdam, Amsterdam, 1105 AZ, The Netherlands
2Amsterdam Brain and Cognition, University of Amsterdam, Amsterdam, 1001 NK, The Netherlands
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Damiaan Denys
1Department of Psychiatry, Amsterdam Neuroscience, Amsterdam UMC, University of Amsterdam, Amsterdam, 1105 AZ, The Netherlands
2Amsterdam Brain and Cognition, University of Amsterdam, Amsterdam, 1001 NK, The Netherlands
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  • Figure 1.
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    Figure 1.

    AEC in the θ (4–8 Hz), α (8–13 Hz), and β (13–30 Hz) frequency bands on the overall task. A, The bars depict average AEC between the NAc (most ventral contact point of the DBS electrode) and 30 randomly selected surface EEG channels, for the left and right NAc separately. B, Topology of the 30 randomly selected surface electrodes.

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    Figure 2.

    Effect of inhibition success on dPTE between right NAc and scalp electrodes. A, dPTE between right NAc and EEG electrode Fpz (large dot) showed a condition effect in the θ-band on successful versus failed inhibition trials (−550−550 ms relative to stop stimulus onset). LMM t values are plotted with small dots indicating tested channels. B, Mean dPTE (arbitrary units, centered) for conditions and patients separately. Positive and negative values indicate cortex→NAc and NAc→cortex information flow, respectively. Error bars indicate SEM. C, Post hoc sliding window analysis showed the effect was highest just before stop stimulus onset (time = 0). Condition effect t values (solid line) were smoothed and plotted on the left y-axis, whereas the right y-axis reflects centered smoothed dPTE intercepts (dashed lines) for the separate conditions, with negative values again indicating effective connectivity from the NAc toward the cortex and vice versa. Since dPTE was calculated for a sliding window, with each dot representing 500 ms, the approximately −290−290 ms shown on the x-axis represents the entire −550- to 550-ms trial length.

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    Figure 3.

    PSD modulation following response on failed inhibition versus correct go trials. Power is expressed in decibel (dB). Error bars indicate SEM. Greater θ power increase following motor response on failed inhibition compared with correct go trials (A) in the left NAc and (B) on electrode FCz. C, Greater α power decrease following motor response on failed inhibition compared with correct go trials on electrode PO4. D–F, Power modulation from plots A–C, respectively, visualized for patients separately. CG and FI refer to correct go and failed inhibition conditions, respectively. *** p < 0.0005 before and 0.002 after Bonferroni correction, ** p < 0.001 before and 0.005 after Bonferroni correction, * p < 0.05.

Tables

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    Table 1

    Subject information and SST performance

    IDSexAgeDiagnosisSSRTMean SSDMean RT
    correct go
    Mean RT
    failed
    inhibition
    % Successful
    inhibition
    % Incorrect
    go
    Patient 1F40OCD238653925840581
    Patient 2F22OCD291164473400460
    Patient 3F32OCD305138433412440
    Patient 4F31OCD233587853744602
    Patient 5F63MDD3082716255415313
    Patient 6M55MDD179667840732522
    Patient 7M37SUD232354606486530
    Summary mean (SD)5 F/2 M40 (14.3)255 (47.9)405 (228.4)679 (194.9)594 (176.7)52% (5.6)2% (4.6)
    • SSRT, stop signal reaction time; SSD, stop signal delay; RT, reaction time; F/M, female/male; OCD, obsessive-compulsive disorder; MDD, major depressive disorder; SUD, substance use disorder; SD, standard deviation.

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    Table 2

    Channel availability

    IDIntracranial contact
    points rejecteda
    EEG channels missing
    from selection
    Number of EEG
    channels rejected
    Number of EEG channels
    not recorded
    Patient 1R1AF73, including AF79
    Patient 2R2AF71, including AF79
    Patient 3R1O1, Oz, O26, including O1, Oz, O28
    Patient 4R2Fp268
    Patient 5R106
    Patient 6R0, R1AF710, including AF710
    Patient 748
    • ↵a R = right hemisphere, 0 = most ventral contact point, located in the NAc, 1–2 = contact points one and two places, respectively, more dorsal from the most ventral contact point/NAc.

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    Table 3

    Condition effects in connectivity between NAc and the cortex

    Time-locking: conditionsConnectivity
    measure
    Frequency
    band
    NAc
    hemisphere
    EEGt valuep value
    before
    Bonferroni
    correction
    p value
    after
    Bonferroni
    correction
    Stop: successful vs failed inhibitiondPTEθRFpz−3.700.00300.0120
    Response: failed inhibition vs correct go*AECθRO12.760.04420.1768
    dPTEαLP13.210.02200.0880
    • ↵* Solely significant before Bonferroni correction.

    • View popup
    Table 4

    PSD modulation following motor response on failed inhibition versus correct go trials

    Frequency bandEffectChannelt valuep value before
    Bonferroni correction
    p value after
    Bonferroni correction
    θCondition × timeNAc L3.290.00040.0016
    Condition × timeFCz3.940.00060.0012
    αConditionNAc L1.870.02840.1136*
    Condition × timePO4−3.110.01100.0220
    • ↵* Solely significant before Bonferroni correction.

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Exploring the Role of the Nucleus Accumbens in Adaptive Behavior Using Concurrent Intracranial and Extracranial Electrophysiological Recordings in Humans
Nadine Eijsker, Guido van Wingen, Ruud Smolders, Dirk J. A. Smit, Damiaan Denys
eNeuro 9 November 2020, 7 (6) ENEURO.0105-20.2020; DOI: 10.1523/ENEURO.0105-20.2020

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Exploring the Role of the Nucleus Accumbens in Adaptive Behavior Using Concurrent Intracranial and Extracranial Electrophysiological Recordings in Humans
Nadine Eijsker, Guido van Wingen, Ruud Smolders, Dirk J. A. Smit, Damiaan Denys
eNeuro 9 November 2020, 7 (6) ENEURO.0105-20.2020; DOI: 10.1523/ENEURO.0105-20.2020
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Keywords

  • cortico-striatal connectivity
  • electroencephalography
  • intracranial EEG
  • spectral power
  • stop signal task
  • θ oscillations

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