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Rewarding choice options typically contain multiple components, but neural signals in single brain voxels are scalar and primarily vary up or down. In a previous study, we had designed reward bundles that contained the same two milkshakes with independently set amounts; we had used psychophysics and rigorous economic concepts to estimate two-dimensional choice indifference curves (ICs) that represented revealed stochastic preferences for these bundles in a systematic, integrated manner. All bundles on the same ICs were equally revealed preferred (and thus had same utility, as inferred from choice indifference); bundles on higher ICs (higher utility) were preferred to bundles on lower ICs (lower utility). In the current study, we used the established behavior for testing with functional magnetic resonance imaging (fMRI). We now demonstrate neural responses in reward-related brain structures of human female and male participants, including striatum, midbrain, and medial orbitofrontal cortex (mid-OFC) that followed the characteristic pattern of ICs: similar responses along ICs (same utility despite different bundle composition), but monotonic change across ICs (different utility). Thus, these brain structures integrated multiple reward components into a scalar signal, well beyond the known subjective value coding of single-component rewards. SIGNIFICANCE STATEMENT Rewards have several components, like the taste and size of an apple, but it is unclear how each component contributes to the overall value of the reward. While choice indifference curves (ICs) of economic theory provide behavioral approaches to this question, it is unclear whether brain responses capture the preference and utility integrated from multiple components. We report activations in striatum, midbrain, and orbitofrontal cortex (OFC) that follow choice ICs representing behavioral preferences over and above variations of individual reward components. In addition, the concept-driven approach encourages future studies on natural, multicomponent rewards that are prone to irrational choice of normal and brain-damaged individuals., (Copyright © 2021 Seak, Volkmann et al.)

We describe a new measure of Granger causality, componential Granger causality, and show how it can be applied to the identification of the directionality of influences between brain areas with functional neuroimaging data. Componential Granger causality measures the effect of y on x, but allows interaction effects between y and x to be measured. In addition, the terms in componential Granger causality sum to 1, allowing causal effects to be directly compared between systems. We show using componential Granger causality analysis applied to an fMRI investigation that there is a top-down attentional effect from the anterior dorsolateral prefrontal cortex to the orbitofrontal cortex when attention is paid to the pleasantness of a taste, and that this effect depends on the activity in the orbitofrontal cortex as shown by the interaction term. Correspondingly there is a top-down attentional effect from the posterior dorsolateral prefrontal cortex to the insular primary taste cortex when attention is paid to the intensity of a taste, and this effect depends on the activity of the insular primary taste cortex as shown by the interaction term. Componential Granger causality thus not only can reveal the directionality of effects between areas (and these can be bidirectional), but also allows the mechanisms to be understood in terms of whether the causal influence of one system on another depends on the state of the system being causally influenced. Componential Granger causality measures the full effects of second order statistics by including variance and covariance effects between each time series, thus allowing interaction effects to be measured, and also provides a systematic framework within which to measure the effects of cross, self, and noise contributions to causality. The findings reveal some of the mechanisms involved in a biased activation theory of selective attention., (Copyright © 2011 Elsevier Inc. All rights reserved.)

To provide a fundamental basis for understanding decision-making and decision confidence, we analyze a neuronal spiking attractor-based model of decision-making. The model predicts probabilistic decision-making with larger neuronal responses and larger functional magnetic resonance imaging (fMRI) blood-oxygen-level-dependent (BOLD) responses on correct than on error trials because the spiking noise-influenced decision attractor state of the network is consistent with the external evidence. Moreover, the model predicts that the neuronal activity and the BOLD response will become larger on correct trials as the discriminability ΔI increases and confidence increases and will become smaller as confidence decreases on error trials as ΔI increases. Confidence is thus an emergent property of the model. In an fMRI study of an olfactory decision-making task, we confirm these predictions for cortical areas including medial prefrontal cortex and the cingulate cortex implicated in choice decision-making, showing a linear increase in the BOLD signal with ΔI on correct trials, and a linear decrease on error trials. These effects were not found in a control area, the orbitofrontal cortex, where reward value useful for the choice is represented on a continuous scale but that is not implicated in the choice itself. This provides a unifying approach to decision-making and decision confidence and to how spiking-related noise affects choice, confidence, synaptic and neuronal activity, and fMRI signals.

To provide a neurobiological basis for understanding decision-making and decision confidence, we describe and analyze a neuronal spiking attractor-based model of decision-making that makes predictions about synaptic and neuronal activity, the fMRI BOLD response, and behavioral choice as a function of the easiness of the decision, and thus decision confidence. The spiking network model predicts probabilistic decision-making with faster and larger neuronal responses on easy versus difficult choices, that is as the discriminability DeltaI between the choices increases, and these and the synaptic currents in turn predict larger BOLD responses as the discriminability increases. Confidence, which increases with discriminability, thus emerges from the firing rates of the decision-making neurons in the choice attractor network. In two fMRI studies, we confirm these predictions by showing that brain areas such as medial prefrontal cortex area 10 implicated in choice decision-making between pleasant stimuli have BOLD activations linearly related to the easiness of both olfactory and warm pleasantness choices. Further, this signature is not found in orbitofrontal cortex areas that represent on a continuous scale the value of the stimuli, but are not implicated in the choice itself. This provides a unifying and fundamental approach to decision-making and decision confidence, and to how spiking-related noise in the brain affects choice, confidence, synaptic and neuronal activity, and fMRI signals., (Copyright 2010 Elsevier Inc. All rights reserved.)

When an economic decision is taken, it is between goals with different values, and the values must be on the same scale. Here, we used functional MRI to search for a brain region that represents the subjective pleasantness of two different rewards on the same neural scale. We found activity in the ventral prefrontal cortex that correlated with the subjective pleasantness of two fundamentally different rewards, taste in the mouth and warmth on the hand. The evidence came from two different investigations, a between-group comparison of two independent fMRI studies, and from a within-subject study. In the latter, we showed that neural activity in the same voxels in the ventral prefrontal cortex correlated with the subjective pleasantness of the different rewards. Moreover, the slope and intercept for the regression lines describing the relationship between activations and subjective pleasantness were highly similar for the different rewards. We also provide evidence that the activations did not simply represent multisensory integration or the salience of the rewards. The findings demonstrate the existence of a specific region in the human brain where neural activity scales with the subjective pleasantness of qualitatively different primary rewards. This suggests a principle of brain processing of importance in reward valuation and decision-making., (Copyright (c) 2010 Elsevier Inc. All rights reserved.)

The palatability and pleasantness of the sensory properties of foods drive food selection and intake and may contribute to overeating and obesity. Oral fat texture can make food palatable and pleasant. To analyze its neural basis, we correlated humans' subjective reports of the pleasantness of the texture and flavor of a high- and low-fat food with a vanilla or strawberry flavor, with neural activations measured with functional magnetic resonance imaging. Activity in the midorbitofrontal and anterior cingulate cortex was correlated with the pleasantness of oral fat texture and in nearby locations with the pleasantness of flavor. The pregenual cingulate cortex showed a supralinear response to the combination of high fat and pleasant, sweet flavor, implicating it in the convergence of fat texture and flavor to produce a representation of highly pleasant stimuli. The subjective reports of oral fattiness were correlated with activations in the midorbitofrontal cortex and ventral striatum. The lateral hypothalamus and amygdala were more strongly activated by high- versus low-fat stimuli. This discovery of which brain regions track the subjective hedonic experience of fat texture will help to unravel possible differences in the neural responses in obese versus lean people to oral fat, a driver of food intake.

Relative reward value is important for the choice between a set of available rewards, and absolute reward value for stable and consistent economic choice. It is unclear whether in the human brain subjective absolute value representations can be dissociated from relative reward value representations. Using fMRI, we investigated how the subjective pleasantness of an odor is influenced by whether the odor is presented in the context of a relatively more pleasant or less pleasant odor. We delivered two of a set of four odors separated by a delay of 6 s, with the instruction to rate the pleasantness of the second odor, and searched for brain regions where the activations were correlated with the absolute pleasantness rating of the second odor, and for brain regions where the activations were correlated with the difference in pleasantness of the second from the first odor, that is, with relative pleasantness. Activations in the anterolateral orbitofrontal cortex tracked the relative subjective pleasantness, whereas activations in the anterior insula tracked the relative subjective unpleasantness. In contrast, in the medial and midorbitofrontal cortex activations tracked the absolute pleasantness of the stimuli. Thus, both relative and absolute subjective value signals which provide important inputs to decision-making processes about which stimulus to choose are separately and simultaneously represented in the human brain.

Decoding and information theoretic techniques were used to analyze the predictions that can be made from functional magnetic resonance neuroimaging data on individual trials. The subjective pleasantness produced by warm and cold applied to the hand could be predicted on single trials with typically in the range 60-80% correct from the activations of groups of voxels in the orbitofrontal and medial prefrontal cortex and pregenual cingulate cortex, and the information available was typically in the range 0.1-0.2 (with a maximum of 0.6) bits. The prediction was typically a little better with multiple voxels than with one voxel, and the information increased sublinearly with the number of voxels up to typically seven voxels. Thus the information from different voxels was not independent, and there was considerable redundancy across voxels. This redundancy was present even when the voxels were from different brain areas. The pairwise stimulus-dependent correlations between voxels, reflecting higher-order interactions, did not encode significant information. For comparison, the activity of a single neuron in the orbitofrontal cortex can predict with 90% correct and encode 0.5 bits of information about whether an affectively positive or negative visual stimulus has been shown, and the information encoded by small numbers of neurons is typically independent. In contrast, the activation of a 3 x 3 x 3-mm voxel reflects the activity of approximately 0.8 million neurons or their synaptic inputs and is not part of the information encoding used by the brain, thus providing a relatively poor readout of information compared with that available from small populations of neurons.

How does selective attention to affect influence sensory processing? In a functional magnetic resonance imaging investigation, when subjects were instructed to remember and rate the pleasantness of a jasmine odor, activations were greater in the medial orbito-frontal and pregenual cingulate cortex than when subjects were instructed to remember and rate the intensity of the odor. When the subjects were instructed to remember and rate the intensity, activations were greater in the inferior frontal gyrus. These top-down effects occurred not only during odor delivery but started in a preparation period after the instruction before odor delivery, and continued after termination of the odor in a short-term memory period. Thus, depending on the context in which odors are presented and whether affect is relevant, the brain prepares itself, responds to, and remembers an odor differently. These findings show that when attention is paid to affective value, the brain systems engaged to prepare for, represent, and remember a sensory stimulus are different from those engaged when attention is directed to the physical properties of a stimulus such as its intensity. This differential biasing of brain regions engaged in processing a sensory stimulus depending on whether the cognitive demand is for affect-related versus more sensory-related processing may be an important aspect of cognition and attention. This has many implications for understanding the effects not only of olfactory but also of other sensory stimuli.

How does selective attention to affect influence sensory processing? In an fMRI investigation, when subjects were instructed to remember and rate the pleasantness of a taste stimulus, 0.1 M monosodium glutamate, activations were greater in the medial orbitofrontal and pregenual cingulate cortex than when subjects were instructed to remember and rate the intensity of the taste. When the subjects were instructed to remember and rate the intensity, activations were greater in the insular taste cortex. An interaction analysis showed that this dissociation of taste processing, depending on whether attention to pleasantness or intensity was relevant, was highly significant (P < 0.0002). Thus, depending on the context in which tastes are presented and whether affect is relevant, the brain responds to a taste differently. These findings show that, when attention is paid to affective value, the brain systems engaged to represent the sensory stimulus of taste are different from those engaged when attention is directed to the physical properties of a stimulus such as its intensity. This differential biasing of brain regions engaged in processing a sensory stimulus, depending on whether the cognitive demand is for affect-related vs. more sensory-related processing, may be an important aspect of cognition and attention. This has many implications for understanding the effects not only of taste but also of other sensory stimuli.

Many affective stimuli are hedonically complex mixtures containing both pleasant and unpleasant components. To investigate whether the brain represents the overall affective value of such complex stimuli, or the affective value of the different components simultaneously, we used functional magnetic resonance imaging to measure brain activations to a pleasant odor (jasmine), an unpleasant odor (indole), and a mixture of the two that was pleasant. In brain regions that represented the pleasantness of the odors such as the medial orbitofrontal cortex (as shown by activations that correlated with the pleasantness ratings), the mixture produced activations of similar magnitude to the pleasant jasmine, but very different from the unpleasant indole. These regions thus emphasize the pleasant aspects of the mixture. In contrast, in regions representing the unpleasantness of odors such as the dorsal anterior cingulate and midorbitofrontal cortex the mixture produced activations that were relatively further from the pleasant component jasmine and closer to the indole. These regions thus emphasize the unpleasant aspects of the mixture. Thus mixtures that are found pleasant can have components that are separately pleasant and unpleasant, and the brain can separately and simultaneously represent the positive and negative hedonic value of a complex affective stimulus that contains both pleasant and unpleasant olfactory components. This type of representation may be important for affective decision making in the brain in that separate representations of different affective components of the same sensory stimulus may provide the inputs for making a decision about whether to choose the stimulus or not.

Abstract: Warm and cold stimuli have affective components such as feeling pleasant or unpleasant, and these components may have survival value, for approach to warmth and avoidance of cold may be reinforcers or goals for action built into us during evolution to direct our behaviour to stimuli that are appropriate for survival. Understanding the brain processing that underlies these prototypical reinforcers provides a direct approach to understanding the brain mechanisms of emotion. In an fMRI investigation in humans, we showed that the mid-orbitofrontal and pregenual cingulate cortex and the ventral striatum have activations that are correlated with the subjective pleasantness ratings made to warm (41 °C) and cold (12 °C) stimuli, and combinations of warm and cold stimuli, applied to the hand. Activations in the lateral and some more anterior parts of the orbitofrontal cortex were correlated with the unpleasantness of the stimuli. In contrast, activations in the somatosensory cortex and ventral posterior insula were correlated with the intensity but not the pleasantness of the thermal stimuli. A principle thus appears to be that processing related to the affective value and associated subjective emotional experience of thermal stimuli that are important for survival is performed in different brain areas to those where activations are related to sensory properties of the stimuli such as their intensity. This conclusion appears to be the case for processing in a number of sensory modalities, and the finding with such prototypical stimuli as warm and cold provides strong support for this principle. [Copyright &y& Elsevier]