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. 2012 May 23;32(21):7146-57.
doi: 10.1523/JNEUROSCI.4821-11.2012.

Your goal is mine: unraveling mimetic desires in the human brain

Maël Lebreton  1 , Shadia Kawa, Baudouin Forgeot d'Arc, Jean Daunizeau, Mathias Pessiglione
Affiliations

Your goal is mine: unraveling mimetic desires in the human brain

Maël Lebreton et al. J Neurosci. .

Abstract

The spread of desires among individuals is widely believed to shape motivational drives in human populations. However, objective evidence for this phenomenon and insights into the underlying brain mechanisms are still lacking. Here we show that participants rated objects as more desirable once perceived as the goals of another agent's action. We then unravel the mechanisms underpinning such goal contagion, using functional neuroimaging. As expected, observing goal-directed actions activated a parietofrontal network known as the mirror neuron system (MNS), whereas subjective desirability ratings were represented in a ventral striatoprefrontal network known as the brain valuation system (BVS). Crucially, the induction of mimetic desires through action observation involved the modulation of BVS activity through MNS activity. Furthermore, MNS-BVS effective connectivity predicted individual susceptibility toward mimetic desires. We therefore suggest that MNS-BVS interaction represents a fundamental mechanism explaining how nonverbal behavior propagates desires without the need for explicit, intentional communication.

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Figures

Figure 1.
Figure 1.
Behavioral tasks. A, The desirability rating task. Successive screens displayed in one trial are shown from left to right with durations in milliseconds. Subjects had to rate the object featured in the video by moving a cursor along an analog scale. The object was taken as the goal of an action in the G condition but not in the NG condition. Each object had an identical, yet differently colored, counterpart with which it formed a pair. Within each pair, one object was featured in a G video and the other in an NG video. The two objects of a pair were always presented in the first and second halves of the same experimental session. Between the two versions of the task (A and B), the conditions (G and NG) assigned to the two objects were swapped. In the example illustrated, the green candy was the G object in version A but the NG object in version B, and vice versa for the yellow candy. To eliminate color preferences at the group level, half the subjects performed version A and the other half performed version B. B, The recognition task. Subjects had to select the “old” object, which meant the object that had been featured in the videos (either G or NG) shown during the rating task. Every choice contained one old and one “new” object. In the illustrated example, the correct answer would be green for the choice on the right and yellow for the choice on the left.
Figure 2.
Figure 2.
The MDE. Histograms illustrate the MDE, defined as the difference in Z-scored desirability ratings between G and NG objects. Error bars indicate intersubject SEM. *p < 0.05, **p < 0.01, ***p < 0.001; paired t test. A, Overall MDE obtained in the five groups of participants. Group 5 (filled bar) corresponds to the subjects who were scanned using fMRI while performing the task. MDE of individual subjects in this group are shown above the bars. B, MDE calculated separately for the two objects of a pair. Filled and empty bars indicate objects that were presented during the first and second parts of an experimental session, respectively. C, MDE obtained in Group 5 for the different types of objects presented in the videos. D, MDE obtained in Group 5 for the different categories of videos. G videos (filled bars on the left) contained objects that were moved (G_M) or not (G_NM). NG videos (empty bars on the right) contained a human agent (NG_A) or not, with the object moved (NG_M) or not (NG_NM). As indicated with asterisks, all comparisons between G and NG categories were significant (solid lines), whereas no significant difference was found between G or NG subcategories (dashed lines). E, Correlation between MDE and other variables (age, empathy, and eye test scores). The y-axis indicates the MDE (difference in Z-scored desirability rating between G and NG objects). Scatter plots show the MDE for all individuals. No correlation was significant (tested using robust regression).
Figure 3.
Figure 3.
ROIs isolated from group-level activations. SPMs were obtained using GLM1 (in Materials and Methods). A, Contrasts of interest. Top, MNS was isolated with the contrast between goal-directed and nongoal-directed actions (G and NG videos). Bottom, BVS was isolated with the parametric modulation by desirability ratings. B, Contrasts of no interest. Top, Occipitotemporal regions activated during videos presenting some movement. Bottom, Occipitotemporal regions activated during NG videos featuring a human agent. Areas shown in gray/black on glass brains and in red/yellow on slices showed significant group-level random effect (p < 0.05 after correction for multiple comparisons at the cluster level). The [x, y, z] coordinates of the different maxima refer to the Montreal Neurological Institute (MNI) space. Slices were taken in the different ROIs, along planes orthogonal to the lines indicated on glass brains. Blue, MNS; green, BVS. C, MNS activations presented separately for the different categories of videos. Regression coefficients were estimated by deconvolution of the hemodynamic response to video display and extracted from ROIs centered on PMC and PL group-level maxima. G videos (filled bars on the left) contained objects that were moved (G_M) or not moved (G_NM). NG videos (empty bars on the right) contained a human agent (NG_A) or not, with the object moved (NG_M) or not (NG_NM). For both regions, all comparisons between NG and G categories remained significant or bordered significance (all p < 0.06, paired t test). Error bars indicate intersubject SEM.
Figure 4.
Figure 4.
Neural correlates of the MDE. A, Information encoded in the different ROIs. Regression coefficients were estimated using GLM2 parametric modulators. G/NG (dotted bars): binary variable that signaled objects being taken as goals. Average rating (empty bars): mean rating over current and paired objects. Differential rating (filled bars): difference between current object and average rating. Error bars indicate intersubject SEM. *p < 0.05, **p < 0.01, ***p < 0.001; one-sample t test. SPM was obtained from the conjunction between G/NG contrast and modulation by differential rating. Areas shown in black on glass brains and in white on slices showed significant group-level random effect (p < 0.001, one-sample t test; uncorrected, minimum of 10 voxels). Sagittal and coronal slices were taken at the global maximum of interest (in the premotor cortex). The [x, y, z] coordinates of the maximum refer to the Montreal Neurological Institute space. B, Comparison between GLM in the different ROIs. Bars indicate the probability of different models estimated using BMS. The model space explored in the BMS is illustrated in the table above the bars. Models could include or not include the G/NG contrast and could decompose or not decompose the desirability ratings into differential (Diff) and average ratings. +, Regressor included in the GLM.
Figure 5.
Figure 5.
Network architecture. A, Illustration of alternative DCMs. In all models, the driving input (red) was a boxcar function over the video-viewing period, parametrically modulated by the experimental condition (1 for goal, 0 for nongoal objects). The different models account for different levels of branching, from a full parallel (model 1) to a serial caudorostral transfer of information (model 9). B, Results of the BMS procedure used to identify the most probable model.
Figure 6.
Figure 6.
Direction of information transfer. Against the caudorostral linear model selected by previous model comparison (model A), we tested the reverse order (model B) and the inversion of the BVS (green) and MNS (blue) regions (model C). A, Illustration of alternative DCMs. B, Results of the BMS procedure. For the winning model (left), the mean ± SD of posterior distributions obtained for the different modulation and connectivity coefficients are indicated. All coefficients were statistically significant at the group level. G/NG: video-viewing period modulated by the experimental condition (1 for goal, 0 for nongoal objects).
Figure 7.
Figure 7.
Interindividual differences. A, Correlation between brain activation and MDE. Brain activation corresponds to the contrast between G and NG. MDE corresponds to the difference in Z-scored desirability ratings between G and NG objects. The activation map results from a group-level, between-subject regression of G/NG contrast against behavioral MDE. Areas shown in gray/black on glass brains and in red/yellow on slices showed significant group-level random effects (p < 0.05 after clusterwise FWE correction for multiple comparisons). The [x, y, z] coordinates of the different maxima refer to the Montreal Neurological Institute space. Slices were taken at the maximum of interest, along planes indicated by blue lines on glass brains. The graph illustrates robust regression of behavioral MDE against G/NG contrast extracted from the maximum of interest in the VS. B, Correlation between connectivity measures extracted from the best DCM and VS activation in the G/NG contrast. The graph illustrates robust regression of VS response to G/NG against the PMC–VS connectivity coefficient (yellow).
Figure 8.
Figure 8.
Functional connectivity model. Between the inputs (G or NG video) and outputs (desirability ratings), ROIs belonging to the mirror neuron system (PL and PMC) and to the brain valuation system (VS and VMPFC) were ordered along a caudorostral axis. Arrows indicate that a given node (experimental variable or brain activity) explains a significant part of the next node variance that is not explained by previous nodes. Histograms indicate the trial-by-trial regression coefficients obtained for the link between two successive nodes of the model, while controlling for the preceding nodes. Error bars indicate intersubject SEM. ***p < 0.001; one-sample t test.
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