Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection

Abstract

Theories of incentive motivation attempt to capture the way in which objects and events in the world can acquire high motivational value and drive behavior, even in the absence of a clear biological need. In addition, for an individual to select the most appropriate goal, the incentive values of competing desirable objects need to be defined and compared. The present study examined the neural substrates by which appetitive incentive value influences prospective goal selection, using positron emission tomographic neuroimaging in humans. Sated subjects were shown a series of restaurant menus that varied in incentive value, specifically tailored for each individual, and in half the trials, were asked to make a selection from the menu. The amygdala was activated by high-incentive menus regardless of whether a choice was required. Indeed, activity in this region varied as a function of individual subjective ratings of incentive value. In contrast, distinct regions of the orbitofrontal cortex were recruited both during incentive judgments and goal selection. Activity in the medial orbital cortex showed a greater response to high-incentive menus and when making a choice, with the latter activity also correlating with subjective ratings of difficulty. Lateral orbitofrontal activity was observed selectively when participants had to suppress responses to alternative desirable items to select their most preferred. Taken together, these data highlight the differential contribution of the amygdala and regions within the orbitofrontal cortex in a neural system underlying the selection of goals based on the prospective incentive value of stimuli, over and above homeostatic influences.

Figure 1.

Subject-rated behavioral measures. A, Average subject ratings (with SEM bars) of incentive value of menu items in each experimental condition. The rating scale ranged from 1 to 5, with higher scores indicating greater incentive value for menu items. High-incentive conditions were rated as being of a significantly greater incentive value than low-incentive conditions (for both choice and nonchoice comparisons: Wilcoxon z = 3.06, p < 0.005). B, Average subject ratings of the difficulty of making choices relating to menu items in the high- and low-incentive categories. The rating scale ranged from 1 to 5, with lower scores indicating a greater difficulty (Diff.) in selecting a goal. Subjects found it significantly more difficult to make choices regarding high-incentive menu items than low-incentive items (Wilcoxon z = 2.47, p < 0.05).

Figure 2.

Significant rCBF changes in the main effect contrast of incentive value. A, A region of the left amygdala (x = -16, y = -4, z = -14) showed increased rCBF in the high-incentive condition. A similar region of the left amygdala (x = -16, y = -6, z = -18) showed a significant covariation of activity with subject-rated incentive value of the menu items (see Fig. 4 A). B, A region of the left medial orbitofrontal cortex (x = -8, y = 44, z = -20) also showed increased rCBF in the high-incentive condition.

Figure 3.

Significant rCBF changes in the main effect contrast of choice (A and C) and in the interaction between incentive value and choice (B). A, An area of left medial orbitofrontal cortex (x = -8, y = 36, z = 16) showed significantly greater rCBF in choice trials over no-choice trials. This peak is in a location similar to the one observed for the main effect contrast of incentive value (Fig. 2 B). B, A region of the right lateral orbitofrontal cortex (x = 48, y = 52, z = -14) showed increased activity for the incentive value × choice interaction, specifically when subjects selected between high-incentive alternatives. C, Significant changes in rCBF were also seen in the medial striatum (x = 16, y = 14, z = 4) in the main effect contrast of choice.

Figure 4.

Correlations between rCBF and subject-rated behavioral measures. Open circles, Low incentive condition; filled circles, high incentive condition. A, rCBF in the amygdala (x = -16, y = -6, z = -18) showed a significant covariation with the subjects' own ratings of the incentive value of menu items such that the greater the incentive value rating the greater the rCBF (Spearman's rho = 0.28). B, rCBF in the left medial orbitofrontal cortex (x = -14, y = 42, z = -24) covaried significantly with choice difficulty (x-axis: greater choice difficulty is indicated by a lower rating). The more difficult the subjects rated the selection, the greater the rCBF in this brain region (Spearman's rho = -0.39).