Shared Neural Mechanisms for the Evaluation of Intense Sensory Stimulation and Economic Reward, Dependent on Stimulation-Seeking Behavior

Abstract

Why are some people strongly motivated by intense sensory experiences? Here we investigated how people encode the value of an intense sensory experience compared with economic reward, and how this varies according to stimulation-seeking preference. Specifically, we used a novel behavioral task in combination with computational modeling to derive the value individuals assigned to the opportunity to experience an intense tactile stimulus (mild electric shock). We then examined functional imaging data recorded during task performance to see how the opportunity to experience the sensory stimulus was encoded in stimulation-seekers versus stimulation-avoiders. We found that for individuals who positively sought out this kind of sensory stimulation, there was common encoding of anticipated economic and sensory rewards in the ventromedial prefrontal cortex. Conversely, there was robust encoding of the modeled probability of receiving such stimulation in the insula only in stimulation-avoidant individuals. Finally, we found preliminary evidence that sensory prediction error signals may be positively signed for stimulation-seekers, but negatively signed for stimulation-avoiders, in the posterior cingulate cortex. These findings may help explain why high intensity sensory experiences are appetitive for some individuals, but not for others, and may have relevance for the increased vulnerability for some psychopathologies, but perhaps increased resilience for others, in high sensation-seeking individuals.

Significance statement: People vary in their preference for intense sensory experiences. Here, we investigated how different individuals evaluate the prospect of an unusual sensory experience (electric shock), compared with the opportunity to gain a more traditional reward (money). We found that in a subset of individuals who sought out such unusual sensory stimulation, anticipation of the sensory outcome was encoded in the same way as that of monetary gain, in the ventromedial prefrontal cortex. Further understanding of stimulation-seeking behavior may shed light on the etiology of psychopathologies such as addiction, for which high or low sensation-seeking personality has been identified as a risk factor.

Keywords: addiction; decision-making; impulsivity; individual differences; sensation-seeking; value.

Figure 1.

Stimulation-seeking task and summary of prescan and in-scanner behavior. A, Stimulation-seeking task. Participants first learned the points values associated with different abstract choice stimuli or CSs (acquisition phase). Half the choice stimuli then became associated with the chance of receiving MES to the hand (became CS+s, P(MES|CS+) = 0.75), while the other half had no additional sensory consequences (became CS−s, P(MES|CS−) = 0). Observing how the opportunity to receive this additional intense tactile stimulation affected participants' choice during these test-phase trials thus allowed derivation of the precise value individuals assigned to the opportunity to receive the extrasensory stimulation (θ). B, Individual choice functions fit to test-phase data from four representative participants, ranging from strongly stimulation-seeking (large positive θ value; top) to strongly stimulation-avoiding (large negative θ value; bottom). A leftward shift in the curve denotes assignment of positive additional value to the opportunity to experience the MES, and a rightward shift a negative value, with the gradient reflecting an individual's choice stochasticity parameter, β. C, Relationship between value assigned to opportunity to experience the MES and self-reported sensation-seeking score (SSS-V-R total score; r = 0.391, p = 0.048). D, Relationship between MES value (i.e., θ) and relative choice reaction time for MES-associated (CS+) versus non-MES-associated (CS−) stimuli [reaction time (RT) effect calculated as median RT_CS+ − median RT_CS−; r = −0.543, p = 0.004]. E, Change in θ values across blocks inside the scanner, illustrated separately for stimulation-seeking (SS; overall θ > 0, N = 8) and stimulation-avoiding (SA; overall θ < 0, N = 18) individuals. F, Proportionate choice of CSs according to their points value, averaged across all acquisition-phase (points learning) trials. In this initial phase (completed before entering the scanner), all CSs were pitted against each other repeatedly in a tournament design. On each trial, participants chose between two CSs, and were then awarded the points value of their chosen CS. Overall proportionate choice of each CS is therefore taken as an index of learning about their points (economic) value. G, Mean “shock knowledge” ratings (ratings on a VAS ranging from “no chance of shock” at −300 to “chance of shock” at +300) for CS+ (MES-associated) and CS− (non-MES-associated) stimuli (ratings were completed following completion of initial shock-learning trials, before entering the scanner). H, Relationship between mean change in VAS “liking” rating of CS+s following introduction of the MES (before entering the scanner), and MES value (θ) calculated from all scanner trials. Error bars represent SEM; dotted lines represent 95% confidence intervals; N = 26. **p < 0.001.

Figure 2.

Effects of individual preference for the MES on BOLD signal when choosing MES-associated versus non-MES-associated stimuli in the vmPFC, vS, and insula. A, Significant positive effects of θ value (valued assigned to opportunity to receive the MES) on BOLD signal when choosing MES-associated (CS+) as opposed to non-MES-associated (CS−) stimuli in the left vmPFC and head of the caudate, bilaterally. B, Significant negative effect of θ value on BOLD signal when choosing CS+ compared with CS− stimuli in the insula, bilaterally. Color bars represent t values. Scatter plots represent mean β estimates extracted from CS+ versus CS− contrast images across whole a priori ROIs (A) and at peak voxel coordinates identified from the group-level contrast (B), plotted against individual θ values.

Figure 3.

Common encoding of the economic and MES-association of choice stimuli in the vmPFC and insula, depending on MES preference. A, Conjunction analysis revealed that a region in the vmPFC cluster identified as showing increasing activity with increasing points value of chosen CSs also showed positive modulation by individual θ value when choosing MES-associated (as opposed to non-MES-associated) stimuli. B, Conjunction analysis revealed that insula clusters identified as showing increasing activity with decreasing points value of chosen CSs also showed negative modulation according to θ value when choosing MES-associated (as opposed to non-MES-associated) stimuli. Color bars represent t values. Scatter plots and bar charts show individual parameter estimates from the CS+ versus CS− contrast, extracted at peak voxels identified from the positive (A) and negative (B) points value group-level contrasts, plotted against θ values. SS, Stimulation-seeking (θ > 0); SA, stimulation-avoiding (θ < 0). Error bars represent SEM. **p = 0.008, *p = 0.015.

Figure 4.

Common encoding of modeled MES-predictedive value and negative economic value in low stimulation-seekers. A, Plot of modeled internal probability of receiving the MES for each CS (SAV_CS), for a representative participant (left). Across all participants, the SAV of the chosen CS on each trial was represented in BOLD signal in the right insula (right). B, Conjunction analysis revealed that an insular region identified as showing increasing activity with decreasing economic value of chosen stimuli showed positive coding of SAV_CS in stimulation-avoiding, but not stimulation-seeking, individuals, during the decision period. C, BOLD signal extracted from the peak voxel identified from the positive points-value contrast (i.e., a region significantly positively encoding the economic value of chosen CSs, located in the vmPFC) revealed marginally greater encoding of SAV in stimulation-seekers, compared with stimulation-avoiders. Color bars represent t values. Bar charts represent parameter estimates extracted from the SAV contrast images, extracted at peak insula voxel coordinates from the negative points-value contrast (A) and the positive points-value contrast (B). SS, Stimulation-seeking (θ > 0); SA, stimulation-avoiding (θ < 0). Error bars represent SEM. *p = 0.012, ∧p = 0.052.

Figure 5.

SPE signals may be positively signed for stimulation-seekers, but negatively signed for stimulation-avoiders, in the PCC. Color bar represents t values. Bar chart represents parameter estimates extracted from SPE contrast images, extracted at peak voxel coordinates from the contrast between high and low stimulation-seekers, when masked by voxels sensitive to SPE signals across the whole group. SS, Stimulation-seeking (θ > 0); SA, stimulation-avoiding (θ < 0). Error bars represent SEM. **p < 0.001.