The role of the posterior temporal and medial prefrontal cortices in mediating learning from romantic interest and rejection.

Romantic interest or rejection can be powerful incentives not merely for their emotional impact, but for their potential to transform, in a single interaction, what we think we know about another person--or ourselves. Little is known, though, about how the brain computes expectations for, and learns from, real-world romantic signals. In a novel "speed-dating" paradigm, we had participants meet potential romantic partners in a series of 5-min "dates," and decide whether they would be interested in seeing each partner again. Afterward, participants were scanned with functional magnetic resonance imaging while they were told, for the first time, whether that partner was interested in them or rejected them. Expressions of interest and rejection activated regions previously associated with "mentalizing," including the posterior superior temporal sulcus (pSTS) and rostromedial prefrontal cortex (RMPFC); while pSTS responded to differences from the participant's own decision, RMPFC responded to prediction errors from a reinforcement-learning model of personal desirability. Responses in affective regions were also highly sensitive to participants' expectations. Far from being inscrutable, then, responses to romantic expressions seem to involve a quantitative learning process, rooted in distinct sources of expectations, and encoded in neural networks that process both affective value and social beliefs.

Dorsomedial prefrontal cortex mediates rapid evaluations predicting the outcome of romantic interactions.

Humans frequently make real-world decisions based on rapid evaluations of minimal information; for example, should we talk to an attractive stranger at a party? Little is known, however, about how the brain makes rapid evaluations with real and immediate social consequences. To address this question, we scanned participants with functional magnetic resonance imaging (fMRI) while they viewed photos of individuals that they subsequently met at real-life "speed-dating" events. Neural activity in two areas of dorsomedial prefrontal cortex (DMPFC), paracingulate cortex, and rostromedial prefrontal cortex (RMPFC) was predictive of whether each individual would be ultimately pursued for a romantic relationship or rejected. Activity in these areas was attributable to two distinct components of romantic evaluation: either consensus judgments about physical beauty (paracingulate cortex) or individualized preferences based on a partner's perceived personality (RMPFC). These data identify novel computational roles for these regions of the DMPFC in even very rapid social evaluations. Even a first glance, then, can accurately predict romantic desire, but that glance involves a mix of physical and psychological judgments that depend on specific regions of DMPFC.

Human dorsal striatum encodes prediction errors during observational learning of instrumental actions.

The dorsal striatum plays a key role in the learning and expression of instrumental reward associations that are acquired through direct experience. However, not all learning about instrumental actions require direct experience. Instead, humans and other animals are also capable of acquiring instrumental actions by observing the experiences of others. In this study, we investigated the extent to which human dorsal striatum is involved in observational as well as experiential instrumental reward learning. Human participants were scanned with fMRI while they observed a confederate over a live video performing an instrumental conditioning task to obtain liquid juice rewards. Participants also performed a similar instrumental task for their own rewards. Using a computational model-based analysis, we found reward prediction errors in the dorsal striatum not only during the experiential learning condition but also during observational learning. These results suggest a key role for the dorsal striatum in learning instrumental associations, even when those associations are acquired purely by observing others.

When giving is good: ventromedial prefrontal cortex activation for others' intentions.

In social decision-making, people care both about others' outcomes and their intentions to help or harm. How the brain integrates representations of others' intentions with their outcomes, however, is unknown. In this study, participants inferred others' decisions in an economic game during functional magnetic resonance imaging. When the game was described in terms of donations, ventromedial prefrontal cortex (VMPFC) activation increased for inferring generous play and decreased for inferring selfish play. When the game was described in terms of individual savings, however, VMPFC activation did not distinguish between strategies. Distinct medial prefrontal regions also encoded consistency with situational norms. A separate network, including right temporoparietal junction and parahippocampal gyrus, was more activated for inferential errors in the donation than in the savings condition. These results demonstrate that neural responses to others' generosity or selfishness depend not only on their actions but also on their perceived intentions.

Bottom-up and top-down processes in emotion generation: common and distinct neural mechanisms.

Emotions are generally thought to arise through the interaction of bottom-up and top-down processes. However, prior work has not delineated their relative contributions. In a sample of 20 females, we used functional magnetic resonance imaging to compare the neural correlates of negative emotions generated by the bottom-up perception of aversive images and by the top-down interpretation of neutral images as aversive. We found that (a) both types of responses activated the amygdala, although bottom-up responses did so more strongly; (b) bottom-up responses activated systems for attending to and encoding perceptual and affective stimulus properties, whereas top-down responses activated prefrontal regions that represent high-level cognitive interpretations; and (c) self-reported affect correlated with activity in the amygdala during bottom-up responding and with activity in the medial prefrontal cortex during top-down responding. These findings provide a neural foundation for emotion theories that posit multiple kinds of appraisal processes and help to clarify mechanisms underlying clinically relevant forms of emotion dysregulation.

Available alternative incentives modulate anticipatory nucleus accumbens activation.

A reward or punishment can seem better or worse depending on what else might have happened. Little is known, however, about how neural representations of an anticipated incentive might be influenced by the available alternatives. We used event-related FMRI to investigate the activation in the nucleus accumbens (NAcc), while we varied the available alternative incentives in a monetary incentive delay task. Some task blocks included only uncertain gains and losses; others included the same uncertain gains and losses intermixed with certain gains and losses. The availability of certain gains and losses increased NAcc activation for uncertain losses and decreased the difference between uncertain gains and losses. We suggest that this pattern of activation can result from reference point changes across blocks, and that the worst available loss may serve as an important anchor for NAcc activation. These findings imply that NAcc activation represents anticipated incentive value relative to the current context of available alternative gains and losses.

Neural systems supporting the control of affective and cognitive conflicts.

Although many studies have examined the neural bases of controlling cognitive responses, the neural systems for controlling conflicts between competing affective responses remain unclear. To address the neural correlates of affective conflict and their relationship to cognitive conflict, the present study collected whole-brain fMRI data during two versions of the Eriksen flanker task. For these tasks, participants indicated either the valence (affective task) or the semantic category (cognitive task) of a central target word while ignoring flanking words that mapped onto either the same (congruent) or a different (incongruent) response as the target. Overall, contrasts of incongruent > congruent trials showed that bilateral dorsal ACC, posterior medial frontal cortex, and dorsolateral pFC were active during both kinds of conflict, whereas rostral medial pFC and left ventrolateral pFC were differentially active during affective or cognitive conflict, respectively. Individual difference analyses showed that separate regions of rostral cingulate/ventromedial pFC and left ventrolateral pFC were positively correlated with the magnitude of response time interference. Taken together, the findings that controlling affective and cognitive conflicts depends upon both common and distinct systems have important implications for understanding the organization of control systems in general and their potential dysfunction in clinical disorders.

Valence and salience contribute to nucleus accumbens activation.

Different accounts of nucleus accumbens (NAcc) function have emphasized its role in representing either valence or salience during incentive anticipation. In an event-related FMRI experiment, we independently manipulated valence and salience by cuing participants to anticipate certain and uncertain monetary gains and losses. NAcc activation correlated with both valence and salience. On trials with certain outcomes, NAcc activation increased for anticipated gains and decreased for anticipated losses. On trials with uncertain outcomes, NAcc activation increased for both anticipated gains and losses but did not differ between them. These findings suggest that NAcc activation separately represents both valence and salience, consistent with its hypothesized role in appetitive motivation.

The lure of the unknown.

Using event-related fMRI, Bunzeck and Düzel show that midbrain regions putatively housing dopamine cell bodies activate more for novel pictures than for negative pictures, pictures requiring a motor response, or repeated pictures. These findings indicate that midbrain regions preferentially respond to novelty and suggest that novelty can serve as its own reward.

The neural correlates of direct and reflected self-knowledge.

Socrates said that in order to lead a balanced life one must, "know thyself." In two fMRI experiments, the present study examined the mechanisms mediating two ways in which the self can be known: through direct appraisals (i.e., an individual's own self-beliefs) and reflected appraisals (i.e., an individual's perception of how others view him or her). Experiment 1 examined the common and distinct neural bases of direct appraisals of the self, close others, and normative judgments of trait desirability. All three judgment types activated medial prefrontal cortex (MPFC) to a similar degree. Experiment 2 examined the common and distinct neural bases of (1) direct appraisals of self, a close other or a non-close other, and (2) reflected appraisals made from the perspective of a close or a non-close other. Consistent with Experiment 1, all judgment types activated MPFC. Direct appraisals of the self as compared to others more strongly recruited MPFC and right rostrolateral PFC. Direct appraisals as compared to reflected appraisals recruited regions associated with a first-person perspective (posterior cingulate), whereas reflected as compared to direct appraisals recruited regions associated with emotion and memory (insula, orbitofrontal, and temporal cortex). These results support models suggesting that MPFC mediates meta-cognitive processes that may be recruited for direct and reflected self appraisals depending upon the demands of a specific task.

Individual differences in trait rumination and the neural systems supporting cognitive reappraisal.

Cognitive reappraisal can alter emotional responses by changing one's interpretation of a situation's meaning. Functional neuroimaging has revealed that using cognitive reappraisal to increase or decrease affective responses involves left prefrontal activation and goal-appropriate increases or decreases in amygdala activation (Ochsner, Bunge, Gross, & Gabrieli, 2002; Ochsner, Ray, et al., 2004). The present study was designed to examine whether patterns of brain activation during reappraisal vary in relation to individual differences in trait rumination, which is the tendency to focus on negative aspects of one's self or negative interpretations of one's life. Individual differences in rumination correlated with increases in amygdala response when participants were increasing negative affect and with greater decreases in prefrontal regions implicated in self-focused thought when participants were decreasing negative affect. Thus, the propensity to ruminate may reflect altered recruitment of mechanisms that potentiate negative affect. These findings clarify relations between rumination and emotion regulation processes and may have important implications for mood and anxiety disorders.

Functional magnetic resonance imaging of reward prediction.

PURPOSE OF REVIEW: Technical and conceptual advances in functional magnetic resonance imaging now allow visualization of real-time changes in oxygenation of deep subcortical regions, leading to rapid advances in scientific characterization of the neural substrates that underlie reward prediction in humans. RECENT FINDINGS: Neuroimaging research over the past year has focused on determining the necessary neural substrates for reward prediction. SUMMARY: While the orbitofrontal cortex has long been implicated in modality-specific reward representation, the ventral striatum (particularly the nucleus accumbens) may play a role in modality-independent representations of predicted reward. On the other hand, the mesial prefrontal cortex appears to play a role in representing reward prediction error and the dorsal caudate in linking reward to behavior. Theoretically, future studies will need to establish the specificity of these responses to reward versus punishment and anticipation versus outcome. Clinically, current findings suggest that patients can predict reward without a prefrontal cortex, but should experience difficulty correcting their behavior when reward predictions are violated.

For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion.

Functional neuroimaging studies examining the neural bases of the cognitive control of emotion have found increased prefrontal and decreased amygdala activation for the reduction or down-regulation of negative emotion. It is unknown, however, (1) whether the same neural systems underlie the enhancement or up-regulation of emotion, and (2) whether altering the nature of the regulatory strategy alters the neural systems mediating the regulation. To address these questions using functional magnetic resonance imaging (fMRI), participants up- and down-regulated negative emotion either by focusing internally on the self-relevance of aversive scenes or by focusing externally on alternative meanings for pictured actions and their situational contexts. Results indicated (1a) that both up- and down-regulating negative emotion recruited prefrontal and anterior cingulate regions implicated in cognitive control, (1b) that amygdala activation was modulated up or down in accord with the regulatory goal, and (1c) that up-regulation uniquely recruited regions of left rostromedial PFC implicated in the retrieval of emotion knowledge, whereas down-regulation uniquely recruited regions of right lateral and orbital PFC implicated in behavioral inhibition. Results also indicated that (2) self-focused regulation recruited medial prefrontal regions implicated in internally focused processing, whereas situation-focused regulation recruited lateral prefrontal regions implicated in externally focused processing. These data suggest that both common and distinct neural systems support various forms of reappraisal and that which particular prefrontal systems modulate the amygdala in different ways depends on the regulatory goal and strategy employed.

Comparison of spiral-in/out and spiral-out BOLD fMRI at 1.5 and 3 T.

Spiral-in/out functional magnetic resonance imaging (fMRI) methods acquire one image before the echo time (TE) and a second image after TE during each scan. Weighted combination of the two images provides a time series with reduced susceptibility dropout in frontal and medial temporal regions as well as increased signal-to-noise ratio (SNR) in regions of uniform cortex. In this study, task activation with the spiral-in/out method was compared to that with conventional spiral-out acquisitions at two field strengths (1.5 and 3.0 T) using episodic memory encoding, verbal working memory, and affective processing tasks in eight human volunteers. With the conventional spiral-out sequence, greater signal dropout is observed in lateral and medial prefrontal, amygdalar, and medial temporal regions at 3 T relative to 1.5 T, whereas such dropout at 3 T is reduced or mitigated with the spiral-in/out method. Similarly, activation volumes for frontal, amygdalar, and medial temporal regions are reduced for spiral-out acquisitions relative to spiral-in/out, and this difference is more apparent at 3 T than at 1.5 T. In addition, significant regionally specific increases in Z scores are obtained with the spiral-in/out sequence relative to spiral-out acquisitions at both field strengths. It is concluded the spiral-in/out sequence may provide significant advantages over conventional spiral methods, especially at 3 T.