The neural mechanisms underlying the influence of pavlovian cues on human decision making

Abstract

In outcome-specific transfer, pavlovian cues that are predictive of specific outcomes bias action choice toward actions associated with those outcomes. This transfer occurs despite no explicit training of the instrumental actions in the presence of pavlovian cues. The neural substrates of this effect in humans are unknown. To address this, we scanned 23 human subjects with functional magnetic resonance imaging while they made choices between different liquid food rewards in the presence of pavlovian cues previously associated with one of these outcomes. We found behavioral evidence of outcome-specific transfer effects in our subjects, as well as differential blood oxygenation level-dependent activity in a region of ventrolateral putamen when subjects chose, respectively, actions consistent and inconsistent with the pavlovian-predicted outcome. Our results suggest that choosing an action incompatible with a pavlovian-predicted outcome might require the inhibition of feasible but nonselected action-outcome associations. The results of this study are relevant for understanding how marketing actions can affect consumer choice behavior as well as for how environmental cues can influence drug-seeking behavior in addiction.

Figure 1.

Illustration of the three different trial types in this study. a, Pavlovian trial. A visual shape stimulus was presented at the center of the screen for 1.75 s followed by a fixation cross for 3 s. The liquid outcome corresponding to the stimulus was then delivered with a probability of 50%. One second was allotted for consumption, and the interval between trials varied uniformly between 1 and 5 s. b, Instrumental trial. Two of the four squares at the bottom of the screen changed color from gray to brown for 1.75 s during which time subjects were instructed to push one of the buttons. The liquid outcome corresponding to their response was delivered after 3 s, with a probability of 50%. One second was allotted for consumption, and the interval between trials varied uniformly between 1 and 5 s. c, Transfer trial. A visual shape stimulus was presented simultaneously with two squares changing color. Subjects were instructed to press one of the corresponding buttons. Timing was similar to the pavlovian and instrumental trials; however, no outcomes were delivered during these trials.

Figure 2.

Behavior during training and test sessions. a, Mean pleasantness ratings for visual cue stimuli after the training sessions, plotted by outcome pairing. The cues paired with the neutral outcome were rated as significantly less pleasant than the cues paired with reward outcomes (paired t test, t₍₂₂₎ = −3.0840; p < 0.01). b, Pupil diameter in response to visual cues. The peak amplitude is significantly smaller for the cues paired with reward outcomes for the 16 subjects who showed reliable amplitude changes after cue presentation (paired t test, t₍₁₅₎ = 2.4173; p < 0.05). c, Choice behavior during the second session of instrumental trials, above cue invariant responding (50%). Plotted are responses during trials in which subjects chose between a reward outcome and the neutral outcome. Subjects were significantly more likely to choose the action leading to the reward outcome (one-sided paired t test, t₍₂₂₎ = 1.8399; p < 0.05). d, Choice data binned into five 10-trial bins. There is no significant linear trend across the session (linear regression of the percentage of compatible choice allocation onto bin number, p = 0.239). Error bars indicate SEM.

Figure 3.

Imaging results from the pavlovian-instrumental transfer (PIT) phase. a, fMRI results from the contrast comparing the outcome-specific transfer trials in which the action compatible with the pavlovian cue is selected to those in which the incompatible action is selected (red, p < 0.01; yellow, p < 0.001). At a threshold of p < 0.001, uncorrected, we find significant activation in the ventrolateral putamen (t₍₂₁₎ = 3.79; p < 0.001, uncorrected; x = 27, y = −3, z = −3) and bilateral pallidum (t₍₂₁₎ = 3.81, p < 0.001, uncorrected, x = 24, y = −18, z = 0; and t₍₂₁₎ = 3.82, p < 0.001, uncorrected, x = −27, y = −15, z = −3). b, Parameter estimates from the peak putamen voxel for each subject for each of the five experimental conditions during the transfer phase [specific compatible (comp), specific incompatible (incomp), pavlovian reward (pav rew) control, pavlovian neutral (pav N) control, and neutral (N) choice control]. Parameter estimates in the specific compatible condition do not differ significantly from any condition other than specific incompatible (paired t tests, p > 0.05). Error bars indicate SEM.