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Research ArticleNegative Results, Sensory and Motor Systems

Pharmacological Dopamine Manipulation Does Not Alter Reward-Based Improvements in Memory Retention during a Visuomotor Adaptation Task

Graziella Quattrocchi, Jessica Monaco, Andy Ho, Friederike Irmen, Wolfgang Strube, Diane Ruge, Sven Bestmann and Joseph M. Galea
eNeuro 15 June 2018, 5 (3) ENEURO.0453-17.2018; https://doi.org/10.1523/ENEURO.0453-17.2018
Graziella Quattrocchi
1Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom
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Jessica Monaco
1Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom
2Brain Connectivity Centre, C. Mondino National Neurological Institute, Pavia I-27100, Italy
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Andy Ho
1Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom
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Friederike Irmen
1Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom
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Wolfgang Strube
1Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom
3Department of Psychiatry and Psychotherapy, Ludwig-Maximilians-University LMU, Munich D-80336, Germany
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Diane Ruge
1Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom
4Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, Technical University Dortmund, Dortmund D-44139, Germany
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Sven Bestmann
1Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom
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Joseph M. Galea
5School of Psychology, University of Birmingham, Birmingham B15 2TT, United Kingdom
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    Figure 1.

    Task and paradigm. A, Task. Participants made 6 cm reaching movements to a target. Visual feedback was perturbed by a 40° clockwise rotation (R) in adaptation phase (rotation). In no vision trials, the cursor and the hand position corresponded but there was no visual feedback. B, Study protocol. Participants completed 72 trials of baseline training with veridical visual feedback, followed by 72 baseline trails with no visual feedback (no vision). Drug (LD/haloperidol/placebo) was then administered and participants waited the corresponding waiting time (1 h for LD or placebo, 2 h for haloperidol). After that, the two baseline blocks were repeated (baseline 2). During adaptation, visual feedback was perturbed 40° clockwise for 216 trials (three blocks). To avoid this starting abruptly at the beginning of a block, the first adaptation block started with six baseline trials with veridical visual feedback, followed by 72 trials with the perturbation. Then, participants were exposed to 216 (retention, three blocks) trials with no perturbation and no visual feedback. Again, to avoid a context change at the beginning of a block, the last adaptation block finished with six retention trials (i.e., total 78 trials in last adaptation block, followed by two retention blocks of 72 trials and one block of 66 trials). C, Hand trajectories toward each target of one representative subject in the R-Pl (violet) and punish-placebo (blue) group. From left to right, Last trial toward each target of baseline 1, last trial toward each target of adaptation, last trial toward each target of retention.

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    Figure 2.

    Reward was associated with greater retention than punishment, independently of LD, haloperidol or placebo. A, Epoch (average across six trials) AD (°) during baseline, adaptation, and retention for the six groups (n = 16 each). The x-axis indicates the number of epochs. The plots represent mean ± SEM. The solid vertical line indicates the wait period after the administration of drug or placebo. The dashed vertical lines indicate the actual beginning and end of first and last adaptation blocks (i.e., the first adaptation block started with six baseline “vision” trials, and the last adaptation block finished with six retention no vision trials). B, Bar graph on the left: average (±SEM) AD (°) for each group during the retention phase. Black dots represent average AD for each participant. The reward groups retained significantly more than the punishment groups [F(1,90) = 9.8, p = 0.002, η2 = 0.098] irrespective of drug status. Bar graph on the right: model parameter A (decay rate, higher values signifying larger retention, average ± SEM) across groups [ART test, F(1,90) = 5.51, p = 0.021, η2 = 0.058]. Black dots represent average decay rate for each participant; *p < 0.05. C, Epoch (average across six trials) AD (°) during baseline, adaptation, and retention for the combined reward groups (n = 48) versus the combined punishment groups (n = 48).

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    Table 1.

    Participants’ characteristics

    R-LDP-LDR-HaloP-HaloR-PlP-Plλ2(5) or F(5,90)p valueEffect size
    BMI21.9 ± 0.723.4 ± 0.923.5 ± 1.421.8 ± 1.122.3 ± 0.721.5 ± 0.50.8350.5280.046
    Education13 (81.3)11 (68.7)15 (93.8)13 (81.3)15 (93.7)12 (75)16.250.2460.024
    MMSE29.7 ± 0.129.4 ± 0.329.4 ± 0.329.7 ± 0.129.5 ± 0.229.7 ± 0.10.600.6990.032
    FAB17.6 ± 0.217.6 ± 0.117.1 ± 0.417.6 ± 0.117.6 ± 0.117.7 ± 0.10.890.4950.047
    Stroop E0.4 ± 0.20.7 ± 0.30.5 ± 0.21.5 ± 0.50.4 ± 0.21 ± 0.31.870.1090.099
    Stroop T4.6 ± 0.94.2 ± 1.33.9 ± 0.95.5 ± 1.75.5 ± 0.75 ± 2.10.270.9280.016
    AES-S28.4 ± 1.326 ± 1.527.9 ± 1.531 ± 1.628.7 ± 1.530 ± 1.61.430.2210.074
    BDI3.3 ± 0.92.9 ± 13.3 ± 1.16 ± 1.73.7 ± 1.15.2 ± 1.31.010.4220.053
    SP3.7 ± 0.73.4 ± 0.54.8 ± 0.64.1 ± 0.63.8 ± 0.73.7 ± 0.70.560.7320.030
    SR4.8 ± 0.63.7 ± 0.55.2 ± 0.65.3 ± 0.54.4 ± 0.63.8 ± 0.71.440.2180.074
    Money18.3 ± 0.418.1 ± 0.617.7 ± 0.618 ± 0.218 ± 0.418.9 ± 0.30.710.6190.038
    Success rate435 (12.6)454 (13.1)419 (12.1)407 (11.8)454 (13.1)463 (13.4)6.440.2660.129
    • Categorical values are indicated as number and percentages (%), numeric values as mean ± SEM. Comparison between proportions is made with χ2 test, comparison between means with one-way ANOVA or Kruskal–Wallis (MMSE, FAB, Stroop, BDI) test. Effect size is provided as phi for χ2 test, partial η for ANOVA, and ε2 for Kruskal–Wallis. R-LD, n = 16; P-LD, n = 16; R-Halo, n = 16; P-Halo, n = 16; R-Pl, n = 16; P-Pl, n = 16; Education, participants with ≥15 years of education; BMI, body mass index (kg/m2); MMSE, mini-mental state examination; FAB, frontal assessment battery; AES-S, apathy evaluation scale, self-administered version; BDI, Beck depression inventory; SP, sensitivity to punishment; SR, sensitivity to reward; Money, GBP (£) received at the end of the session; Success rate, number of trials in which the maximum amount of points was received (i.e., four points in the reward groups and zero points in the punishment groups).

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    Table 2.

    RTs, MTs, and baseline AD across groups

    R-LDP-LDR-HaloP-HaloR-PlP-PlANOVA
    Baseline 1
        RT317 ± 14333 ± 17352 ± 10350 ± 11387 ± 29333 ± 13F(5,90) = 2.01, p = 0.085, η2 = 0.100
        MT286 ± 14261 ± 10303 ± 6269 ± 8278 ± 13278 ± 11F(5,90) = 1.76, p = 0.129, η2 = 0.089
        AD-0.7 ± 0.3-1.5 ± 0.5-0.9 ± 0.4-1.2 ± 0.3-1.2 ± 0.5-0.9 ± 0.2F(5,90) = 0.64, p = 0.670, η2 = 0.034
    Baseline 2
        RT305 ± 22318 ± 18346 ± 9353 ± 10374 ± 30287 ± 14F(5,90) = 3.07, p = 0.013, η2 = 0.146
        MT249 ± 8259 ± 14269 ± 7269 ± 6255 ± 11237 ± 7F(5,90) = 0.71, p = 0.140, η2 = 0.087
        AD-0.7 ± 0.3-0.4 ± 0.5-0.3 ± 0.5-0.9 ± 0.3-1.2 ± 0.2-0.9 ± 0.3F(5,90) = 0.78, p = 0.569, η2 = 0.041
    Adaptation
        RT298 ± 21327 ± 17343 ± 8368 ± 15371 ± 25321 ± 23Fb : F(1,90) = 0.005, p = 0.941, η2 = 0.0
    D : F(2,90) = 2.74, p = 0.070, η2 = 0.06
    Fb*D : F(2,90) = 2.69, p = 0.073, η2 = 0.06
        MT243 ± 6264 ± 15277 ± 11279 ± 7270 ± 15264 ± 13Fb : F(1,90) = 0.32, p = 0.573, η2 = 0.004
    D : F(2,90) = 2.23, p = 0.114, η2 = 0.05
    Fb*D : F(2,90) = 0.69, p = 0.502, η2 = 0.01
    Retention
        RT292 ± 24288 ± 14351 ± 8348 ± 10338 ± 23289 ± 12Fb : F(1,90) = 2.01, p = 0.160, η2 = 0.02
    D : F(2,90) = 6.78, p = 0.002, η2 = 0.13
    Fb*D : F(2,90) = 1.31, p = 0.276, η2 = 0.03
        MT227 ± 8232 ± 14262 ± 7250 ± 6245 ± 10231 ± 9Fb : F(1,90) = 0.87, p = 0.353, η2 = 0.01
    D : F(2,90) = 3.92, p = 0.023, η2 = 0.08
    Fb*D : F(2,90) = 0.59, p = 0.554, η2 = 0.01
    • Values depict the mean ± SEM by averaging over consecutive epochs for each participant and group. A one-way ANOVA was used to compare mean values across groups during baseline 1 and baseline 2. A multifactorial ANOVA was used to compare mean values across groups, with feedback (reward*punishment) and drug (LD*haloperidol*placebo) as between-groups factors. R-LD, n = 16; P-LD, n = 16; R-Halo, n = 16; P-Halo, n = 16; R-Pl, n = 16; P-Pl, n = 16; RT, in ms; MT, in ms; AD, °; Fb, feedback; D, drug. Significant results are bold.

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Pharmacological Dopamine Manipulation Does Not Alter Reward-Based Improvements in Memory Retention during a Visuomotor Adaptation Task
Graziella Quattrocchi, Jessica Monaco, Andy Ho, Friederike Irmen, Wolfgang Strube, Diane Ruge, Sven Bestmann, Joseph M. Galea
eNeuro 15 June 2018, 5 (3) ENEURO.0453-17.2018; DOI: 10.1523/ENEURO.0453-17.2018

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Pharmacological Dopamine Manipulation Does Not Alter Reward-Based Improvements in Memory Retention during a Visuomotor Adaptation Task
Graziella Quattrocchi, Jessica Monaco, Andy Ho, Friederike Irmen, Wolfgang Strube, Diane Ruge, Sven Bestmann, Joseph M. Galea
eNeuro 15 June 2018, 5 (3) ENEURO.0453-17.2018; DOI: 10.1523/ENEURO.0453-17.2018
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Keywords

  • adaptation
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