Neural interactions in the human frontal cortex dissociate reward and punishment learning

  1. Etienne Combrisson  Is a corresponding author
  2. Ruggero Basanisi
  3. Maelle CM Gueguen
  4. Sylvain Rheims
  5. Philippe Kahane
  6. Julien Bastin
  7. Andrea Brovelli  Is a corresponding author
  1. Institut de Neurosciences de La Timone, UMR 7289, CNRS, Aix-Marseille Université, France
  2. Univ. Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, France
  3. Department of Functional Neurology and Epileptology, Hospices Civils de Lyon and University of Lyon, France
  4. Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, France
16 figures, 1 table and 1 additional file

Figures

Figure 1 with 2 supplements
intracerebral EEG (iEEG) implantation, behavioral task, and computational modeling.

(A) Anatomical location of intracerebral electrodes across the 16 epileptic patients. Anterior insula (aINS, n=75), dorsolateral prefrontal cortex (dlPFC, n=70), lateral orbitofrontal cortex (lOFC, …

Figure 1—figure supplement 1
Single subject anatomical repartition.

(A) Number of unique subjects per brain region and per pair of brain regions (B) Number of bipolar derivations per subject and per brain region.

Figure 1—figure supplement 2
Single-subject estimation of prediction errors.

Single-subject trial-wise reward prediction error (PE) (Reward prediction error, RPE - blue) and punishment PE (PPE - red), ±95% confidence interval.

Figure 2 with 2 supplements
Local mixed encoding of reward and punishment prediction error signals.

(A) Time-courses of mutual information (MI in bits) estimated between the gamma power and the reward (blue) and punishment (red) prediction error (PE) signals. The solid line and the shaded area …

Figure 2—figure supplement 1
Local encoding of prediction error signals within the gamma band.

(A) Distribution of information in the anterior insula (aINS), dorsolateral prefrontal cortex (dlPFC), lateral orbitofrontal cortex (lOFC), and vmPFC about the R/punishment prediction error (PPE) in …

Figure 2—figure supplement 2
Inter-subjects reproducibility of local encoding of prediction error (PE) signals.

Time-courses of the proportion of unique subjects having at least one bipolar derivation with a significant encoding (p<0.05, cluster-based correction, non-parametric randomization across epochs) of …

Figure 3 with 1 supplement
Encoding of prediction error (PE) signals occurs with redundancy-dominated subsystems.

Dynamic interaction information (II in bits) within- (A) and between-regions (B) about the RPE (IIRPE) and PPE (IIPPE) are plotted in blue and red. Significant clusters of IIRPE and IIPPE are …

Figure 3—figure supplement 1
Inter-subjects reproducibility of redundant interactions about prediction error (PE) signals.

Time-courses of the proportion of unique subjects having at least one pair of bipolar derivation with significant interaction information (p<0.05, cluster-based correction, non-parametric …

Figure 4 with 2 supplements
Contextual modulation of information transfer.

Time courses of transfer entropy (TE, in bits) from the anterior insula (aINS) to the dorsolateral prefrontal cortex (dlPFC) (aINS→dlPFC) and from the vmPFC to the lateral orbitofrontal cortex …

Figure 4—figure supplement 1
Optimal delay interval for maximizing information transfer.

Modulation of transfer entropy (TE in bits), estimated across all pairs of contacts per participant, as a function of the delay between source and target areas. The delay represents the number of …

Figure 4—figure supplement 2
Contextual modulation of the information transfer.

Time courses of transfer entropy (TE, in bits) are estimated during the rewarding condition (TERew in blue) and punishing condition (TEPun in red). Significant differences (p<0.05, cluster-based …

Figure 5 with 3 supplements
Synergistic interactions about the full prediction error (PE) signals between recordings of the dlPFC and vmPFC.

(A) Dynamic interaction information (II in bits) between the dorsolateral prefrontal cortex (dlPFC) and vmPFC about the full prediction error (IIdlPFC-vmPFC). Hot and cold colors indicate synergy- …

Figure 5—figure supplement 1
Cortico-cortical interactions about the full prediction error (PE) signals.

Dynamic interaction information (II in bits) between-regions about the full prediction error (IIPE). Hot and cold colors indicate synergy- and redundancy-dominated interactions about the full PE. …

Figure 5—figure supplement 2
Interaction information is binned according to the local specificity.

We binned the II about the full prediction error (PE) (i.e. by concatenating the reward prediction error, RPE and punishment prediction error, PPE) according to the local specificity of the bipolar …

Figure 5—figure supplement 3
Local specificity does not fully determine the type of interactions.

We performed a simulation to demonstrate that synergistic interactions can emerge between two regions with the same specificity. For example, consider one region that locally encodes early trials of …

Summary of findings.

The four nodes represent the investigated regions, namely the anterior insula (aINS), the dorsolateral and ventromedial parts of the prefrontal cortex (dlPFC and vmPFC, and the lateral orbitofrontal …

Author response image 1
Single subject anatomical repartition.

(A) Number of unique subject per brain region and per pair of brain regions. (B) Number of bipolar derivations per subject and per brain region.

Author response image 2
Single-subject estimation of predictions errors.

Single-subject trial-wise reward PE (RPE - blue) and punishment PE (PPE - red), ± 95% confidence interval.

Author response image 3
Author response image 4
Local specificity does not fully determine the type of interactions.

Within-area local encoding of PE using the mutual information (MI, in bits) for regions X and Y and between-area interaction information (II, in bits) leading to (A) redundant interactions and (B) …

Author response image 5
Single-subject estimation of predictions errors.

Single-subject trial-wise reward PE (RPE - blue) and punishment PE (PPE - red), ± 95% confidence interval.

Author response image 6
Single-subject estimation of predictions errors per pair of stimuli.

Single-subject trial-wise reward PE (RPE - blue) and punishment PE (PPE - red).

Author response image 7
MI between gamma activity and R/PPE using early and late trials.

Time courses of MI estimated between the gamma power and both RPE (blue) and PPE (red) using either early or late trials (first and second row, respectively). Horizontal thick lines represent …

Author response image 8
Single subject anatomical repartition.

(A) Number of unique subject per brain region and per pair of brain regions. (B) Number of bipolar derivations per subject and per brain region.

Author response image 9
Author response image 10
Inter-subjects reproducibility of redundant interactions about PE signals.

Time-courses of proportion of subjects having at least one pair of bipolar derivation with a significant interaction information (p<0.05, cluster-based correction, non-parametric randomization …

Tables

Table 1
Results of the one-sample t-test performed against 0.
T-valuep-valuep-value(FDR corrected)dofCI 95%
IIPPE-RPE28590.007**0.015*34[6.5e-05, 3.9e-04]
IIMixed28410.008**0.015*33[5.4e-05, 3.3e-04]
IIPPE-PPE1,250.26670.35565[–7.1e-05, 2.1e-04]
IIRPE-RPE07330.49120.49126[–3.1e-05, 5.8e-05]

Additional files

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