Identity-specific coding of future rewards in the human orbitofrontal cortex

Abstract

Nervous systems must encode information about the identity of expected outcomes to make adaptive decisions. However, the neural mechanisms underlying identity-specific value signaling remain poorly understood. By manipulating the value and identity of appetizing food odors in a pattern-based imaging paradigm of human classical conditioning, we were able to identify dissociable predictive representations of identity-specific reward in orbitofrontal cortex (OFC) and identity-general reward in ventromedial prefrontal cortex (vmPFC). Reward-related functional coupling between OFC and olfactory (piriform) cortex and between vmPFC and amygdala revealed parallel pathways that support identity-specific and -general predictive signaling. The demonstration of identity-specific value representations in OFC highlights a role for this region in model-based behavior and reveals mechanisms by which appetitive behavior can go awry.

Keywords: associative learning; multivoxel pattern analysis; olfaction; reward value; ventromedial prefrontal cortex.

Fig. 1.

Experimental design and stimuli. (A, Upper) Hunger ratings and (A, Lower) time to last meal did not differ across days (one-way ANOVAs: hunger, F_{2,28 =} 0.34, P = 0.71; time to last meal, f_2,28 = 0.97, P = 0.39). Note that error bars for SEM (n = 15) are smaller than the symbols. (B) Pictorial representations of the sweet and savory food odor stimuli used in the experiment. (C) Illustration of the two-factorial design of our study, in which value (low vs. high) and identity (sweet vs. savory) could be independently manipulated. (D) Subjects learned to associate each of four odor US with two unique visual CS, resulting in two stimulus sets (counterbalanced across subjects). (E) On each trial of the fMRI task, one of eight CS images was presented, and subjects had to predict either the value of the upcoming US [response options: low (L) and high (H)] or the identity of the upcoming US [response options in this example: strawberry (SB) and potato chips (PC)]. This prediction was followed by a sniff cue and delivery of odor.

Fig. 2.

Pleasantness ratings and breathing data. (A and B) Pleasantness ratings of (A) US and (B) CS were systematically higher for high- vs. low-intensity stimuli (paired t tests). (C) Average sniff responses locked to the sniff cue. (D) Average peak sniff amplitudes. Error bars are SEMs (n = 15). t test (n = 15). *P < 0.05; ^§P = 0.052.

Fig. 3.

OFC represents identity-specific predictive values. (A) Schematic of the searchlight decoding analysis used to reveal identity-specific value codes. Value-related voxel responses (i.e., fMRI signal difference between high- and low-value conditions) were extracted for CS images predicting sweet odors (pink/red colors) and savory odors (blue colors). An SVM was trained to classify the identity of value-related (high vs. low value) response patterns for one set of CS and then, tested on the second set of CS (to ensure that effects were not driven by mere visual features of the CS images). (B and C) Identity-specific value responses were identified in OFC, hippocampus (HIP), and ACC. Display threshold is P < 0.001. (D) Value imbalances between sweet and savory odors have no impact on identity-specific coding (r = 0.08, P = 0.76), suggesting that decoding is not based on residual value differences between the two odor identities.

Fig. 4.

vmPFC represents identity-general predictive values. (A) Schematic of the searchlight decoding analysis used to identify identity-independent value coding. SVM models were trained on activity patterns evoked by the CS images predicting the high- vs. low-value sweet odor and then, tested on patterns evoked by the CS predicting the high- vs. low-value savory odor (and vice versa). (B) Identity-general value in the vmPFC. Display threshold is P < 0.001. (C) Identity-general coding is higher when the imbalance between sweet and savory values is lower (r = −0.68, P = 0.01), further supporting the role of vmPFC in coding identity-general value.

Fig. 5.

Functional networks of general- and identity-specific value coding. (A) Seed regions used in the functional connectivity analyses. (B) Voxels in the amygdala (AMY) show a general value-related change in connectivity with vmPFC. (C) Individual differences in hunger significantly predict value-related connectivity between vmPFC and amygdala (r = 0.58, P = 0.02). (D and E) Regions in the (D) anterior piriform cortex (APC) and (E) ACC show identity-specific value-related connectivity with OFC. Display threshold is P < 0.001.