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Hedonic processing in humans is mediated by an opioidergic mechanism in a mesocorticolimbic system

  1. Christian Buchel  Is a corresponding author
  2. Stephan Miedl
  3. Christian Sprenger
  1. University Medical Center Hamburg-Eppendorf, Germany
Research Communication
Cite this article as: eLife 2018;7:e39648 doi: 10.7554/eLife.39648
5 figures, 1 data set and 11 additional files

Figures

Figure 1 with 1 supplement
Adapted Monetary Incentive Delay (MID) task trial structure.

An initial cue signaled potential gain for each trial (high/low pleasure erotic picture or high/low monetary reward). After a variable delay, a target briefly appeared. Responding during target display yielded the indicated gain, whereas late or early responses yielded no gain. Target durations were adapted to approximate 67% hit rate for each subject. In case of gain trials volunteers could watch the outcome picture (erotic picture or money) for 1.5 s. In case of loss trials a scrambled image was shown.

https://doi.org/10.7554/eLife.39648.002
Figure 1—figure supplement 1
Behavioral rating data.

Top row: Pleasure and frustration ratings for received and missed monetary rewards. Bottom row: Pleasure and frustration ratings for received and missed erotic picture rewards.

https://doi.org/10.7554/eLife.39648.003
Z-transformed skin conductance responses for anticipation and reward.

Data is shown for n = 14 volunteers during the placebo treatment only, because naloxone is known to directly affect autonomic regulation of SCR (Traore et al., 1998).

https://doi.org/10.7554/eLife.39648.004
Behavioral data shows that the opioid antagonist naloxone significantly reduced ratings for high erotic rewards (dark gray bars).

Frustration ratings for missed erotic rewards show a stronger decrease by naloxone as compared to monetary rewards (right). (* denotes p<0.05; * between bars denote p<0.05 for the interaction).

https://doi.org/10.7554/eLife.39648.005
Figure 4 with 12 supplements
Region of interest brain activity for high versus low erotic picture (dark gray) and high versus low monetary reward (light gray) outcomes shows naloxone related reduced activation for erotic trials.

Under naloxone treatment, activation in the ventral striatum, medial prefrontal cortex lateral orbitofrontal cortex, the amygdala and the hypothalamus is significantly reduced. This reduction is larger for erotic rewards as compared to monetary rewards. Activations for high versus low erotic pictures comparing placebo to naloxone at p<0.005 (uncorrected, t-test) are overlaid on a mean structural image also indicating the predefined volumes of interest (light gray) in the ventral striatum, medial prefrontal cortex and lateral orbitofrontal cortex, amygdala and hypothalamus. (** denotes p<0.05 corrected for multiple comparisons; *p<0.05 uncorrected; * or ** between bars denote p values for the interaction).

https://doi.org/10.7554/eLife.39648.006
Figure 4—figure supplement 1
Region of interest contrasts of brain activity for high versus low erotic picture reward outcome for placebo and naloxone treatment.

**p<0.05 corrected for multiple comparisons; *p<0.05 uncorrected.

https://doi.org/10.7554/eLife.39648.007
Figure 4—figure supplement 2
Region of interest contrasts of brain activity for high versus low monetary reward outcome for placebo and naloxone treatment.
https://doi.org/10.7554/eLife.39648.008
Figure 4—figure supplement 3
Region of interest contrasts of brain activity for high versus low monetary reward anticipation for placebo and naloxone treatment (*p<0.05, uncorrected).
https://doi.org/10.7554/eLife.39648.009
Figure 4—figure supplement 4
Region of interest contrasts of brain activity for high versus low erotic picture reward anticipation for placebo and naloxone treatment.
https://doi.org/10.7554/eLife.39648.010
Figure 4—figure supplement 5
Right ventral striatum (nucleus accumbens) fMRI responses (arbitrary units) for all stimuli (money/erotic, high/low) and time-points (anticipation, outcome: reward, outcome: miss) under placebo (Plac) and naloxone (Nlx).

Error bars represent standard error of the mean.

https://doi.org/10.7554/eLife.39648.011
Figure 4—figure supplement 6
Left ventral striatum (nucleus accumbens) fMRI responses (arbitrary units) for all stimuli (money/erotic, high/low) and time-points (anticipation, outcome: reward, outcome: miss) under placebo (Plac) and naloxone (Nlx).

Error bars represent standard error of the mean.

https://doi.org/10.7554/eLife.39648.012
Figure 4—figure supplement 7
Right lateral orbitofrontal cortex fMRI responses (arbitrary units) for all stimuli (money/erotic, high/low) and time-points (anticipation, outcome: reward, outcome: miss) under placebo (Plac) and naloxone (Nlx).

Error bars represent standard error of the mean.

https://doi.org/10.7554/eLife.39648.013
Figure 4—figure supplement 8
Left lateral orbitofrontal cortex fMRI responses (arbitrary units) for all stimuli (money/erotic, high/low) and time-points (anticipation, outcome: reward, outcome: miss) under placebo (Plac) and naloxone (Nlx).

Error bars represent standard error of the mean.

https://doi.org/10.7554/eLife.39648.014
Figure 4—figure supplement 9
Right amygdala fMRI responses (arbitrary units) for all stimuli (money/erotic, high/low) and time-points (anticipation, outcome: reward, outcome: miss) under placebo (Plac) and naloxone (Nlx).

Error bars represent standard error of the mean.

https://doi.org/10.7554/eLife.39648.015
Figure 4—figure supplement 10
Left amygdala fMRI responses (arbitrary units) for all stimuli (money/erotic, high/low) and time-points (anticipation, outcome: reward, outcome: miss) under placebo (Plac) and naloxone (Nlx).

Error bars represent standard error of the mean.

https://doi.org/10.7554/eLife.39648.016
Figure 4—figure supplement 11
Medial prefrontal cortex fMRI responses (arbitrary units) for all stimuli (money/erotic, high/low) and time-points (anticipation, outcome: reward, outcome: miss) under placebo (Plac) and naloxone (Nlx).

Error bars represent standard error of the mean.

https://doi.org/10.7554/eLife.39648.017
Figure 4—figure supplement 12
Hypothalamus fMRI responses (arbitrary units) for all stimuli (money/erotic, high/low) and time-points (anticipation, outcome: reward, outcome: miss) under placebo (Plac) and naloxone (Nlx).

Error bars represent standard error of the mean.

https://doi.org/10.7554/eLife.39648.018
Positive correlation between naloxone induced decreases in fMRI signal in the hypothalamus and decreases in ratings for erotic rewards.

The more naloxone reduced fMRI signal comparing high versus low erotic rewards during outcome, the more the rating difference between high and low erotic rewards was reduced (See also Table S10). Activations showing this correlation at p<0.005 (uncorrected, t-test) are overlaid on a mean structural image also indicating the predefined volumes of interest (light gray) in the hypothalamus and amygdala.

https://doi.org/10.7554/eLife.39648.019

Data availability

Only freely available data analysis tools were used (SPM, Ledalab). Data are available online via Dryad (http://dx.doi.org/10.5061/dryad.11j304c)."

The following data sets were generated
  1. 1
    Dryad Digital Repository
    1. Buchel Christian
    2. Miedl Stephan
    3. Sprenger Christian
    (2018)
    Data from: Hedonic processing in humans is mediated by an opioidergic mechanism in a mesocorticolimbic system.
    https://doi.org/10.5061/dryad.11j304c

Additional files

Supplementary file 1

Side effects ratings.

Two sided paired Wilcoxon signed rank test comparing mood between naloxone (_nlx) and saline (_nacl) sessions.

https://doi.org/10.7554/eLife.39648.020
Supplementary file 2

Mood ratings.

Two sided paired Wilcoxon signed rank test comparing mood between naloxone (_nlx) and saline (_nacl) sessions.

https://doi.org/10.7554/eLife.39648.021
Supplementary file 3

Rating differences for successful and missed reward trials in the placebo treatment condition.

https://doi.org/10.7554/eLife.39648.022
Supplementary file 4

Effects of Naloxone on pleasure ratings.

Repeated measures ANOVA, Huynh-Feldt nonsphericity correction.

https://doi.org/10.7554/eLife.39648.023
Supplementary file 5

Naloxone effects (relative to placebo) on pleasure ratings.

https://doi.org/10.7554/eLife.39648.024
Supplementary file 6

Coordinates from individual studies to define the center of ROIs.

https://doi.org/10.7554/eLife.39648.025
Supplementary file 7

Naloxone effects (relative to placebo) on the high versus low erotic image outcome contrast.

https://doi.org/10.7554/eLife.39648.026
Supplementary file 8

Naloxone effects (relative to placebo) comparing erotic versus monetary outcomes.

https://doi.org/10.7554/eLife.39648.027
Supplementary file 9

Naloxone effects (relative to placebo) on other contrasts.

https://doi.org/10.7554/eLife.39648.028
Supplementary file 10

Regression analysis relating the change in pleasure ratings to the change in fMRI signal.

https://doi.org/10.7554/eLife.39648.029
Transparent reporting form
https://doi.org/10.7554/eLife.39648.031

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