Neural correlates of specific and general Pavlovian-to-Instrumental Transfer within human amygdalar subregions: a high-resolution fMRI study

Abstract

It is widely held that the interaction between instrumental and Pavlovian conditioning induces powerful motivational biases. Pavlovian-Instrumental Transfer (PIT) is one of the key paradigms demonstrating this effect, which can further be decomposed into a general and specific component. Although these two forms of PIT have been studied at the level of amygdalar subregions in rodents, it is still unknown whether they involve different areas of the human amygdala. Using a high-resolution fMRI (hr-fMRI) protocol optimized for the amygdala in combination with a novel free operant task designed to elicit effects of both general and specific PIT, we demonstrate that a region of ventral amygdala within the boundaries of the basolateral complex and the ventrolateral putamen are involved in specific PIT, while a region of dorsal amygdala within the boundaries of the centromedial complex is involved in general PIT. These results add to a burgeoning literature indicating different functional contributions for these different amygdalar subregions in reward-processing and motivation.

Figure 1.

PIT task illustration. Participants performed an instrumental (a) and a Pavlovian (b) task before performing the PIT task (c). During the instrumental trials, two of the three squares at the bottom of the screen changed color from black to gray for 6 s during which time participants were instructed to press any given button multiple times to get rewarded with food. The food picture corresponding to their response was displayed on one side of the screen for 1 s every 10 presses on average. In the Pavlovian trials, a conditioned stimulus was presented on one side of the screen for 6 s, and the food picture corresponding to the stimulus was displayed on the other side of the screen during the last second of the trial. During the PIT trials, the conditioned stimulus was presented simultaneously with two squares changing color for 6 s. Participants were instructed to press any given key multiple times to get rewarded with food, as in the instrumental trials. In this phase, the area where the food picture was usually displayed was hidden behind a gray square.

Figure 2.

Percentage of number of presses for five 18-trial blocks across all trials. There is no significant linear trend across the session. Error bars indicate SEM.

Figure 3.

Blood oxygen level-dependent (BOLD) signal for the main effect of specific PIT (specific trials > general and neutral trials) in right ventrolateral putamen, using a height threshold of p < 0.005, and a small volume correction significant at p < 0.05 corrected for multiple comparisons.

Figure 4.

Specific and General PIT in the amygdala. a, BOLD signal positively correlating with the magnitude of specific (in green) and general (in red) PIT across participants in the ventral and dorsal amygdalae, respectively, using a height threshold of p < 0.005, with an extent threshold significant at p < 0.05 corrected for multiple comparisons. b, Scatter plot showing the β estimates extracted from a 2 mm sphere centered on the peak voxel within the ventral amygdala correlating with specific PIT against the strength of behavioral specific PIT for each participant. c, Scatter plot showing the β estimates extracted from a 2 mm sphere centered on the peak voxel correlating with general PIT in the dorsal amygdala against the strength of behavioral general PIT for each participant. The plots in c and d were produced using a leave-one-participant-out procedure, thereby avoiding nonindependence issues (see Materials and Methods, Plotting of parameter estimates, for details). d, e, Similar scatter plots as displayed in b, c except that no leave-one-participant-out procedure was used.