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 identityspecific 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.reward value | associative learning | ventromedial prefrontal cortex | olfaction | multivoxel pattern analysis P redictive representations of future outcomes are critical for guiding adaptive behavior. To choose different types of rewards, such as food, shelter, and mates, it is essential that predictive signals contain specific information about the identity of those outcomes. Food rewards differ dramatically in their nutritional composition, and identity-specific cues allow differential foraging depending on current needs of the organism. The absence of precise mappings between predictive reward signals and their intended outcomes would have devastating effects on foodbased decisions.Despite the ecological relevance of outcome-specific predictive coding, which can be observed even in Drosophila (1), most research in human and nonhuman primates has focused on "common currency" signals of economic values in the orbitofrontal cortex (OFC) (2, 3) and ventromedial prefrontal cortex (vmPFC) (4-8). These signals, which by definition are independent of the specific nature of the reward, can be used to compare and choose between alternative outcomes, but are unable to inform expectations about the specific identity of the outcome. For this, identity-specific representations that conjointly represent information about both affective value (how good is it?) and outcome identity (what is it?) are necessary. Recent data suggest that the OFC is involved in signaling information about specific outcomes (9-14). For instance, many OFC neurons signal both the value and the identity of the predicted outcome (12), and OFC lesions diminish the effects of outcome identity (but not general affective value) on conditioned behavior (13).Recent imaging work has also begun to address how the human brain encodes predictive information about rewarding outcomes. One study (9) used a functional magnetic resonance imaging (fMRI) adaptation paradigm to provide evidence for identity-based codes for reward in the OFC. Another investigation (4) used fMRI data from a willingness to pay auction combined with decoding techniques to reveal...

Redefining the Role of Limbic Areas in Cortical Processing

“…It is well established that visual and auditory systems work via predictive coding (e.g., [5], [43–45] in humans, for a review on visual processing see [46]), and there is increasing evidence that the olfactory and gustatory sensory systems work via predictive coding as well ([47–49] in rodents, [50,51] in humans), along with a proposal that somatomotor system works similarly [6–9]. We propose that limbic cortices are at the top of each hierarchical cortical system and send predictions to better-laminated areas.…”

Changing views of emotion regulation and neurobiological models of the mechanism of action of psychotherapy

“…Whereas parietal and temporal association cortices surround visual, auditory, and somatosensory areas, the ventromedial/orbitofrontal cortex and the anterior insula are adjacent to primary olfactory and gustatory areas (Rolls, 2000). Neurophysiological studies in laboratory animals and functional imaging in humans show that associative memory to rewarding or aversive experiences are stored in these areas (Balleine, Leung, & Ostlund, 2011;Gottfried & Zelano, 2011;Howard, Gottfried, Tobler, & Kahnt, 2015;Liljeholm, Tricomi, O'Doherty, & Balleine, 2011;Noonan, Kolling, Walton, & Rushworth, 2012;Parkes, Bradfield, & Balleine, 2015;Rudebeck, Saunders, Prescott, Chau, & Murray, 2013;Schoenbaum, Roesch, Stalnaker, & Takahashi, 2009).…”

Elucidating the underlying components of food valuation in the human orbitofrontal cortex

“…Recent human neuroimaging studies have begun to elaborate functional contributions of OFC in food value computations. Medial OFC encodes value signals independent of identity of food rewards 8 , irrespective of whether the value information is acquired through direct experience or imagination of the consequences of a new experience 20 . On the other hand, lateral OFC encodes value in an identity-specific manner 8,21 .…”

“…Medial OFC encodes value signals independent of identity of food rewards 8 , irrespective of whether the value information is acquired through direct experience or imagination of the consequences of a new experience 20 . On the other hand, lateral OFC encodes value in an identity-specific manner 8,21 . However, it still remains elusive what constituent attributes underlie the construction of food value and how the constituent attributes are represented and integrated in the OFC.…”