Value, Pleasure, and Choice in the Ventral Prefrontal Cortex

Supplementary Material

Value, pleasure, and choice in the ventral prefrontal cortex

Fabian Grabenhorst1 and Edmund T. Rolls2

1 University of Cambridge, Department of Physiology, Development and Neuroscience, Cambridge, UK.

2 Oxford Centre for Computational Neuroscience, Oxford, UK.

Corresponding author: Rolls, E. T. ()

Table S1. Principles of operation of OFC and ACC in reward processing, and their adaptive value

Operational principle / Adaptive value
1. Neural activity in OFC and ACC represents reward value and pleasure on a continuous scale[S1-6]. / This type of representation provides useful inputs for neural attractor networks involved in cost-benefit analysis and decision-making.
2. The identity and intensity of stimuli are represented at earlier cortical stages that send inputs to OFC and ACC: stimuli and objects are first represented, then their reward and affective value is computed in OFC[S1, S7, S8]. / This separation of affective and sensory processing is highly adaptive for it enables us to identify and learn about stimuli independently of whether we currently want them and find them rewarding.
3. Many different rewards are represented close together in OFC and ACC, including taste, olfactory, oral texture, temperature, touch, visual, social, amphetamine induced, and monetary rewards[S3, S9]. / This organization facilitates comparison and common scaling of different rewards by lateral inhibition, and thus provides appropriately scaled inputs for a choice decision-making process [S9].
4. Spatially separate representations of pleasant stimuli (rewards) and unpleasant stimuli (punishers) exist in OFC and ACC[S1, S7]. / This type of organization provides separate and partly independent inputs into brain systems for cost-benefit analysis and decision-making.
5. The value of specific rewards is represented in OFC: different single neurons respond to different combinations of specific taste, olfactory, fat texture, oral viscosity, visual, and face and vocal expression rewards. / This type of encoding provides a reward window on the world that allows not only selection of specific rewards, but also for sensory-specific satiety, a specific reduction in the value of a stimulus after it has been received continuously for a period of time.
6. Both absolute and relative value signals are present in OFC [S10-S13]. / Absolute value is necessary for stable long-term preferences and transitivity[S12]. Being sensitive to relative value may be useful in climbing local reward gradients as in positive contrast effects[S10].
7. Top-down cognitive and attentional factors, originating in lateral prefrontal cortex, modulate reward value and pleasantness in OFC and ACC through biased competition and biased activation[S8, S14-17]. / These top-down effects allow cognition and attention to modulate the first cortical stage of reward processing to influence valuation and economic decision-making.

Supplementary legend to Fig. 2. a. Maps of subjective pleasure in the orbitofrontal cortex (OFC, ventral view) and anterior cingulate cortex (ACC, sagittal view). Yellow: sites where activations correlate with subjective pleasantness. White: sites where activations correlate with subjective unpleasantness. The numbers refer to effects found in specific studies. Taste: 1 [S8], 2 [S14]; odor: 3, 4 [S1]; 5 [S10]; 6, 7 [S18]; 8, 9 [S19]; 10 [S20]; flavor: 11, 12 [S3]; 13 [S8]; 14 [S21]; 15 [S4]; 16 [S22]; oral texture: 17, 18 [S3]; chocolate: 19 [S23]; water: 20 [S24]; wine: 21 [S25]; oral temperature: 22, 23 [S26]; somatosensory temperature: 24, 25 [S7]; the sight of touch: 26, 27 [S27]; facial attractiveness: 28, 29 [S28]; erotic pictures: 30 [S29]; laser-induced pain: 31 [S30].

Supplementary legend to Fig. 3. From valuation to choice in the ventromedial prefrontal cortex. Left: Activations associated with 1: (economic) subjective value during intertemporal choice [S31]; 2: immediate vs delayed choices [S32]; 3 immediate vs delayed primary rewards[S33];4: expected value during probabilistic decision-making [S34]; 5: expected value based on social and experience-based information [S35]; 6: expected value of chosen option [S36]; 7: price differential during purchasing decisions [S37]; 8: willingness to pay [S38]; 9: goal value during decisions about food cues [S39]; 10: choice probability during exploitative choices [S40]; 11: conjunction of stimulus- and action-based value signals [S41]; 12: goal value during decisions about food stimuli [S17]; 13: willingness to pay for different goods [S42]; 14: willingness to pay for lottery tickets [S43]; 15: subjective value of charitable donations [S44]; 16: decision value for exchanging monetary against social rewards [S45]; 17: binary choice vs valuation of thermal stimuli [S2]; 18: binary choice vs valuation of olfactory stimuli [S5]; 19: easy vs difficult choices about thermal stimuli [S46]; 20: easy vs difficult choices about olfactory stimuli [S46]; 21: value of chosen action [S47]; 22: difference in value between choices [S48]; 23: prior correct signal during probabilistic reversal learning [S49]; 24: free vs forced charitable donation choices [S44].It is notable that some of the most anterior activations in VMPFC (activations 17-19) were associated with binary choice during decision-making and not just with valuation during decision-making.

Supplementary references

[S1] Grabenhorst, F., et al. (2007) How pleasant and unpleasant stimuli combine in different brain regions: odor mixtures. Journal of Neuroscience 27, 13532-13540

[S2] Grabenhorst, F., et al. (2008) From affective value to decision-making in the prefrontal cortex. European Journal of Neuroscience 28, 1930-1939

[S3] Grabenhorst, F., et al. (2010) How the brain represents the reward value of fat in the mouth. Cerebral Cortex 20, 1082-1091

[S4] Kringelbach, M.L., et al.(2003) Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. Cerebral Cortex 13, 1064-1071

[S5] Rolls, E.T., et al. (2010) Neural systems underlying decisions about affective odors. Journal of cognitive neuroscience 22, 1069-1082

[S6] Padoa-Schioppa, C. and Assad, J.A. (2006) Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223-226

[S7] Rolls, E.T., et al. (2008) Warm pleasant feelings in the brain. NeuroImage 41, 1504-1513

[S8] Grabenhorst, F., et al. (2008) How cognition modulates affective responses to taste and flavor: top down influences on the orbitofrontal and pregenual cingulate cortices. Cerebral Cortex 18, 1549-1559

[S9] Grabenhorst, F., et al. (2010) A common neural scale for the subjective pleasantness of different primary rewards. NeuroImage 51, 1265-1274

[S10] Grabenhorst, F. and Rolls, E.T. (2009) Different representations of relative and absolute value in the human brain. NeuroImage 48, 258-268

[S11] Tremblay, L. and Schultz, W. (1999) Relative reward preference in primate orbitofrontal cortex. Nature 398, 704-708

[S12] Padoa-Schioppa, C. and Assad, J.A. (2008) The representation of economic value in the orbitofrontal cortex is invariant for changes of menu. Nature neuroscience 11, 95-102

[S13] Elliott, R., et al. (2008) Medial orbitofrontal cortex codes relative rather than absolute value of financial rewards in humans. The European journal of neuroscience 27, 2213-2218

[S14] Grabenhorst, F. and Rolls, E.T. (2008) Selective attention to affective value alters how the brain processes taste stimuli. European Journal of Neuroscience 27, 723-729

[S15] Grabenhorst, F. and Rolls, E.T. (2010) Attentional modulation of affective vs sensory processing: functional connectivity and a top-down biased activation theory of selective attention. Journal of neurophysiology 104, 1649-1660

[S16] Rolls, E.T., et al. (2008) Selective attention to affective value alters how the brain processes olfactory stimuli. Journal of cognitive neuroscience 20, 1815-1826

[S17] Hare, T.A., et al. (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324, 646-648

[S18] Rolls, E.T., et al. (2003) Different representations of pleasant and unpleasant odors in the human brain. European Journal of Neuroscience 18, 695-703

[S19] Anderson, A.K., et al. (2003) Dissociated neural representations of intensity and valence in human olfaction. Nature neuroscience 6, 196-202

[S20] de Araujo, I.E.T., et al.(2005) Cognitive modulation of olfactory processing. Neuron 46, 671-679

[S21] McCabe, C. and Rolls, E.T. (2007) Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain. European Journal of Neuroscience 25, 1855-1864

[S22] de Araujo, I.E.T., et al.(2003) Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. European Journal of Neuroscience 18, 2059-2068

[S23] Rolls, E.T. and McCabe, C. (2007) Enhanced affective brain representations of chocolate in cravers vs non-cravers. European Journal of Neuroscience 26, 1067-1076

[S24] de Araujo, I.E.T., et al.(2003) Human cortical responses to water in the mouth, and the effects of thirst. Journal of neurophysiology 90, 1865-1876

[S25] Plassmann, H., et al. (2008) Marketing actions can modulate neural representations of experienced pleasantness. Proceedings of the National Academy of Sciences of the United States of America 105, 1050-1054

[S26] Guest, S., et al. (2007) Human cortical representation of oral temperature. Physiology and Behavior 92, 975-984

[S27] McCabe, C., et al. (2008) Cognitive influences on the affective representation of touch and the sight of touch in the human brain. Social, Cognitive and Affective Neuroscience 3, 97-108

[S28] O'Doherty, J., et al. (2003) Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia 41, 147-155

[S29] Walter, M., et al. (2008) Distinguishing specific sexual and general emotional effects in fMRI-subcortical and cortical arousal during erotic picture viewing. NeuroImage 40, 1482-1494

[S30] Raij, T.T., et al. (2005) Brain correlates of subjective reality of physically and psychologically induced pain. Proceedings of the National Academy of Sciences of the United States of America 102, 2147-2151

[S31] Kable, J.W. and Glimcher, P.W. (2007) The neural correlates of subjective value during intertemporal choice. Nature neuroscience 10, 1625-1633

[S32] McClure, S.M., et al. (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306, 503-507

[S33] Berns, G.S., et al.(2001) Predictability modulates human brain response to reward. J Neurosci 21, 2793-2798

[S34] Rolls, E.T., et al. (2008) Expected value, reward outcome, and temporal difference error representations in a probabilistic decision task. Cerebral Cortex 18, 652-663

[S35] Behrens, T.E., et al.(2008) Associative learning of social value. Nature 456, 245-249

[S36] Boorman, E.D., et al. (2009) How green is the grass on the other side? Frontopolar cortex and the evidence in favor of alternative courses of action. Neuron 62, 733-743

[S37] Knutson, B., et al. (2007) Neural predictors of purchases. Neuron 53, 147-156

[S38] Plassmann, H., et al. (2007) Orbitofrontal cortex encodes willingness to pay in everyday economic transactions. J Neurosci 27, 9984-9988

[S39] Hare, T.A., et al. (2008) Dissociating the role of the orbitofrontal cortex and the striatum in the computation of goal values and prediction errors. J Neurosci 28, 5623-5630

[S40] Daw, N.D., et al. (2006) Cortical substrates for exploratory decisions in humans. Nature 441, 876-879

[S41] Glascher, J., et al. (2009) Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. Cereb Cortex 19, 483-495

[S42] Chib, V.S., et al. (2009) Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex. J Neurosci 29, 12315-12320

[S43] De Martino, B., et al. (2009) The neurobiology of reference-dependent value computation. J Neurosci 29, 3833-3842

[S44] Hare, T.A., et al. (2010) Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J Neurosci 30, 583-590

[S45] Smith, D.V., et al. (2010) Distinct value signals in anterior and posterior ventromedial prefrontal cortex. J Neurosci 30, 2490-2495

[S46] Rolls, E.T., et al. (2010) Choice, difficulty, and confidence in the brain. NeuroImage 53, 694-706

[S47] Wunderlich, K., et al.(2009) Neural computations underlying action-based decision making in the human brain. Proceedings of the National Academy of Sciences of the United States of America 106, 17199-17204

[S48] FitzGerald, T.H., et al. (2009) The role of human orbitofrontal cortex in value comparison for incommensurable objects. J Neurosci 29, 8388-8395

[S49] Hampton, A.N., et al. (2006) The role of the ventromedial prefrontal cortex in abstract state-based inference during decision making in humans. J Neurosci 26, 8360-8367