Neurobiological and memory models of risky decision making in adolescents versus young adults

Predictions of fuzzy-trace theory and neurobiological approaches are examined regarding risk taking in a classic decision-making task--the framing task--as well as in the context of real-life risk taking. We report the 1st study of framing effects in adolescents versus adults, varying risk and reward, and relate choices to individual differences, sexual behavior, and behavioral intentions. As predicted by fuzzy-trace theory, adolescents modulated risk taking according to risk and reward. Adults showed standard framing, reflecting greater emphasis on gist-based (qualitative) reasoning, but adolescents displayed reverse framing when potential gains for risk taking were high, reflecting greater emphasis on verbatim-based (quantitative) reasoning. Reverse framing signals a different way of thinking compared with standard framing (reverse framing also differs from simply choosing the risky option). Measures of verbatim- and gist-based reasoning about risk, sensation seeking, behavioral activation, and inhibition were used to extract dimensions of risk proneness: Sensation seeking increased and then decreased, whereas inhibition increased from early adolescence to young adulthood, predicted by neurobiological theories. Two additional dimensions, verbatim- and gist-based reasoning about risk, loaded separately and predicted unique variance in risk taking. Importantly, framing responses predicted real-life risk taking. Reasoning was the most consistent predictor of real-life risk taking: (a) Intentions to have sex, sexual behavior, and number of partners decreased when gist-based reasoning was triggered by retrieval cues in questions about perceived risk, whereas (b) intentions to have sex and number of partners increased when verbatim-based reasoning was triggered by different retrieval cues in questions about perceived risk.     

Effort discounting in human nucleus accumbens

A great deal of behavioral and economic research suggests that the value attached to a reward stands in inverse relation to the amount of effort required to obtain it, a principle known as effort discounting. In the present article, we present the first direct evidence for a neural analogue of effort discounting. We used fMRI to measure neural responses to monetary rewards in the human nucleus accumbens (NAcc), a structure previously demonstrated to encode reference-dependent reward information. The magnitude of accumbens activation was found to vary with both reward outcome and the degree of mental effort demanded to obtain individual rewards. For a fixed level of reward, the NAcc was less strongly activated following a high-demand for effort than following a low demand. The magnitude of this effect was noted to correlate with preceding activation in the dorsal anterior cingulate cortex, a region that has been proposed to monitor information-processing demands and to mediate in the subjective experience of effort.     

Aesthetic package design: A behavioral,neural, and psychological investigation

In four experiments, this research sheds light on aesthetic experiences by rigorously investigating behavioral, neural, and psychological properties of package design. We find that aesthetic packages significantly increase the reaction time of consumers' choice responses; that they are chosen over products with well-known brands in standardized packages, despite higher prices; and that they result in increased activation in the nucleus accumbens and the ventromedial prefrontal cortex, according to functional magnetic resonance imaging (fMRI). The results suggest that reward value plays an important role in aesthetic product experiences. Further, a closer look at psychometric and neuroimaging data finds that a paper-and-pencil measure of affective product involvement correlates with aesthetic product experiences in the brain. Implications for future aesthetics research, package designers, and product managers are discussed.     

奖惩对行为抑制及程序阶段中自主生理反应的影响

采用停止信号任务探讨奖惩条件对行为抑制和程序阶段中自主生理反应的影响。结果显示：(1)奖惩组的反应时显著高于控制组, 抑制失败率则显著低于控制组; (2)奖励组与其它两组相比表现出心率显著增加和皮肤电活动显著降低; (3)各生理指标在准备、工作和奖惩阶段中的奖惩差异性显著(4)奖惩条件下皮肤电活动呈现出一致性程序阶段变化。结果表明：奖惩条件均对行为具有抑制作用, 但在自主生理反应上则有显著差异; 各生理指标在准备、工作和奖惩阶段的情绪效价显著; 皮肤电活动的程序阶段变化显著, 但其奖惩效价较为稳定, 很少接受程序阶段变化的影响。     

Approach-withdrawal and the role of the striatum in the temperament of behavioral inhibition

Behavioral inhibition is a temperament characterized in infancy and early childhood by a tendency to withdraw from novel or unfamiliar stimuli. Children exhibiting this disposition, relative to children with other dispositions, are more socially reticent, less likely to initiate interaction with peers, and more likely to develop anxiety over time. Until recently, a dominant model attributed this disposition to reductions in the threshold for engaging the circuitry supporting fear learning, particularly the amygdala. Recent work, however, also has implicated striatal circuitry and other regions that constitute components of a presumed reward system. A series of studies found that behaviorally inhibited adolescents display heightened activation of striatal structures to cues indicating an opportunity to receive reward. This article reviews evidence implicating dual roles for fear and reward circuitry in the expression of behavioral inhibition.     

奖惩对行为抑制能力和自主生理活动影响的时效性

将45名被试随机分配为奖励组、惩罚组和对照组, 实验进程按时间发展过程被分为五阶段, 采用停止信号任务探讨奖惩刺激对行为抑制能力和自主生理活动影响的时效性。结果显示：奖惩刺激对行为反应时和抑制失败率影响仅在第二、三阶段差异显著, 对心率影响的显著差异在第三阶段结束、而对皮电和指温影响的显著差异仍持续到第五阶段。结果表明：奖惩刺激对行为的抑制作用具有时效性, 有效时间内表现为仅奖励能提高行为抑制能力; 奖惩刺激对心率的影响具有时效性, 但对其它生理指标的影响则未显示出时效性。     

阈下奖励调节认知控制的权衡

本研究采用奖励版的AX-CPT任务, 通过控制奖励线索和反馈的呈现方式, 设置出基线、阈上奖励、阈下奖励三种条件, 考察习得的奖励联结和奖励动机能否以潜意识的方式影响认知任务的表现和认知控制的权衡。结果显示：奖励线索只在阈上呈现时提高AX序列的任务表现; 与基线条件相比, 阈上和阈下奖励条件下认知控制的权衡均偏向主动性控制, 且这种偏向在两者间无显著差异。这表明习得的阈下奖励线索可以调节认知控制的权衡, 使被试像阈上奖励时那样偏向主动性控制。     

The reward of a good joke: neural correlates of viewing dynamic displays of stand-up comedy

Humor is enjoyable, yet few studies to date have reported that humor engages brain regions involved in reward processing (i.e., the mesolimbic reward system). Even fewer have investigated socially relevant, dynamic displays of real actors telling jokes. Instead, many studies have focused on responses to static cartoons or written jokes in isolation. In the present investigation, we used functional magnetic resonance imaging (fMRI) to examine brain activation in response to video clips of comedians performing stand-up comedy, a more socially relevant task than reading jokes or cartoons in isolation. Participants watched video clips of eight stand-up comedians, half female/half male, that were prerated by a separate group of participants from the same population as eliciting either high or low levels of amusement, thereby allowing us to control for comedian attributes and comedic style. We found that high-funny clips elicited more activation in several brain regions involved with reward responses, including the nucleus accumbens, caudate, and putamen. A regression with participants’ own ratings of humor revealed similar activity in reward areas as well as in regions involved in theory of mind. These findings indicate that dynamic social displays of humor do engage reward responses. The rewarding nature of humor may help explain why it is so valued socially.     

Reward improves cancellation and restraint inhibition across childhood and adolescence

Inhibitory control allows for the regulation of thought and action and interacts with motivational variables, such as reward, to modify behavior adaptively as environments change. The authors examined the effects of reward on two distinct forms of inhibitory control, cancellation and restraint. Typically developing children and adolescents completed 2 versions of the stop signal task (cancellation and restraint) under 3 reward conditions (neutral, low reward, and high reward), where rewards were earned for successful inhibitory control. Rewards improved both cancellation and restraint inhibition, with similar effects of reward on each form of inhibitory control. Rewards did not alter the speed of response execution in either task, suggesting that rewards specifically altered inhibition processes without influencing processes related to response execution. Adolescents were faster and less variable than children when executing and inhibiting their responses. There were similar developmental effects of reward on the speed of inhibitory control, but group differences were found in terms of accuracy of inhibition in the restraint task. These results clarify how reward modulates two different forms of regulatory behavior in children and adolescents.     

Reward anticipation enhances brain activation during response inhibition

The chance to achieve a reward starts up the required neurobehavioral mechanisms to adapt our thoughts and actions in order to accomplish our objective. However, reward does not equally reinforce everybody but depends on interindividual motivational dispositions. Thus, immediate reward contingencies can modulate the cognitive process required for goal achievement, while individual differences in personality can affect this modulation. We aimed to test the interaction between inhibition-related brain response and motivational processing in a stop signal task by reward anticipation and whether individual differences in sensitivity to reward (SR) modulate such interaction. We analyzed the cognitive–motivational interaction between the brain pattern activation of the regions involved in correct and incorrect response inhibition and the association between such brain activations and SR scores. We also analyzed the behavioral effects of reward on both reaction times for the “go” trials before and after correct and incorrect inhibition in order to test error prediction performance and postinhibition adjustment. Our results show enhanced activation during response inhibition under reward contingencies in frontal, parietal, and subcortical areas. Moreover, activation of the right insula and the left putamen positively correlates with the SR scores. Finally, the possibility of reward outcome affects not only response inhibition performance (e.g., reducing stop signal reaction time), but also error prediction performance and postinhibition adjustment. Therefore, reward contingencies improve behavioral performance and enhance brain activation during response inhibition, and SR is related to brain activation. Our results suggest the conditions and factors that subserve cognitive control strategies in cognitive motivational interactions during response inhibition.     

Behavioral, but not reward, risk modulates activation of prefrontal, parietal, and insular cortices

Risky decisions may involve uncertainty about possible outcomes (i.e., reward risk) or uncertainty about which action should be taken (i.e., behavioral risk). Determining whether different forms of risk have distinct neural correlates is a central goal of neuroeconomic research. In two functional magnetic resonance imaging experiments, subjects viewed shapes that had well-learned response-reward contingencies. Magnitude of a monetary reward was held constant within one experiment, whereas expected value was held constant within the other. Response selection, in the absence of behavioral risk, evoked activation within a broad set of brain regions, as had been found in prior studies. However, behavioral risk additionally modulated activation in prefrontal, parietal, and insular regions, within which no effect of reward risk was observed. Reward delivery, in comparison with omission, evoked increased activity in the ventromedial prefrontal cortex and the nucleus accumbens. We conclude that distinct brain systems are recruited for the resolution of different forms of risk.     

Peers influence adolescent reward processing,but not response inhibition

Most adolescent risk taking occurs in the presence of peers. Prior research suggests that peers alter adolescents’ decision making by increasing reward sensitivity and the engagement of regions involved in the processing of rewards, primarily the striatum. However, the potential influence of peers on the capacity for impulse control, and the associated recruitment of the brain’s control circuitry, has not yet been adequately examined. In the current study, adolescents underwent functional neuroimaging while they completed interleaved rounds of risk-taking and response-inhibition tasks. Social context was manipulated such that the participants believed they were either playing alone and unobserved, or watched by an anonymous peer. Compared to those who completed the tasks alone, adolescents in the peer condition took more risks during the risk-taking task and exhibited relatively heightened activation of the striatum. Activity within this striatal region also predicted individual differences in overall risk taking. In contrast, the presence of peers had no effect on behavioral response inhibition and had minimal impact on the engagement of typical cognitive control regions. In a subregion of the anterior insula engaged mutually by both tasks, activity was again found to be sensitive to social context during the risk-taking task, but not during the response-inhibition task. These findings extend the evidence that the presence of peers biases adolescents towards risk taking by increasing reward sensitivity rather than disrupting cognitive control.     

Reward prospect rapidly speeds up response inhibition via reactive control

Response inhibition is an important cognitive-control function that allows for already-initiated or habitual behavioral responses to be promptly withheld when needed. A typical paradigm to study this function is the stop-signal task. From this task, the stop-signal response time (SSRT) can be derived, which indexes how rapidly an already-initiated response can be canceled. Typically, SSRTs range around 200 ms, identifying response inhibition as a particularly rapid cognitive-control process. Even so, it has recently been shown that SSRTs can be further accelerated if successful response inhibition is rewarded. Since this earlier study effectively ruled out differential preparatory (proactive) control adjustments, the reward benefits likely relied on boosted reactive control. Yet, given how rapidly such control processes would need to be enhanced, alternative explanations circumventing reactive control are important to consider. We addressed this question with an fMRI study by gauging the overlap of the brain networks associated with reward-related and response-inhibition-related processes in a reward-modulated stop-signal task. In line with the view that reactive control can indeed be boosted swiftly by reward availability, we found that the activity in key brain areas related to response inhibition was enhanced for reward-related stop trials. Furthermore, we observed that this beneficial reward effect was triggered by enhanced connectivity between task-unspecific (reward-related) and task-specific (inhibition-related) areas in the medial prefrontal cortex (mPFC). The present data hence suggest that reward information can be translated very rapidly into behavioral benefits (here, within ~200 ms) through enhanced reactive control, underscoring the immediate responsiveness of such control processes to reward availability in general.     

Regulatory interactions of stress and reward on rat forebrain opioidergic and GABAergic circuitry

Palatable food intake reduces stress responses, suggesting that individuals may consume such ?comfort? food as self-medication for stress relief. The mechanism by which palatable foods provide stress relief is not known, but likely lies at the intersection of forebrain reward and stress regulatory circuits. Forebrain opioidergic and gamma-aminobutyric acid ergic signaling is critical for both reward and stress regulation, suggesting that these systems are prime candidates for mediating stress relief by palatable foods. Thus, the present study (1) determines how palatable ?comfort? food alters stress-induced changes in the mRNA expression of inhibitory neurotransmitters in reward and stress neurocircuitry and (2) identifies candidate brain regions that may underlie comfort food-mediated stress reduction. We used a model of palatable ?snacking? in combination with a model of chronic variable stress followed by in situ hybridization to determine forebrain levels of pro-opioid and glutamic acid decarboxylase (GAD) mRNA. The data identify regions within the extended amygdala, striatum, and hypothalamus as potential regions for mediating hypothalamic-pituitary-adrenal axis buffering following palatable snacking. Specifically, palatable snacking alone decreased pro-enkephalin-A (ENK) mRNA expression in the anterior bed nucleus of the stria terminalis (BST) and the nucleus accumbens, and decreased GAD65 mRNA in the posterior BST. Chronic stress alone increased ENK mRNA in the hypothalamus, nucleus accumbens, amygdala, and hippocampus; increased dynorphin mRNA in the nucleus accumbens; increased GAD65 mRNA in the anterior hypothalamus and BST; and decreased GAD65 mRNA in the dorsal hypothalamus. Importantly, palatable food intake prevented stress-induced gene expression changes in subregions of the hypothalamus, BST, and nucleus accumbens. Overall, these data suggest that complex interactions exist between brain reward and stress pathways and that palatable snacking can mitigate many of the neurochemical alterations induced by chronic stress.     

Do orangutans (<Emphasis Type="Italic">Pongo pygmaeus</Emphasis>) know when they do not remember?

Metacognition refers to the ability to monitor and control one’s own cognitive activities such as memory. Although recent studies have raised an interesting possibility that some species of nonhuman animals might possess such skills, subjects often required a numerous number of training trials to acquire the effective use of metacognitive responses. Here, five orangutans (Pongo pygmaeus) were tested whether they were able to escape spatial memory tests when they did not remember the location of preferred reward in a relatively small number of trials. The apes were presented with two identical cups, under one of which the experimenter hid a preferred reward (e.g., two grapes). The subjects were then presented with a third container, “escape response”, with which they could receive a less preferred but secure reward (e.g., one grape). The orangutans as a group significantly more likely selected the escape response when the baiting of the preferred reward was invisible (as compared to when it was visible) and when the hiding locations of the preferred reward were switched (as compared to when they remained unchanged). Even when the escape response was presented before the final presentation of the memory test, one orangutan successfully avoided the test in which she would likely err. These findings indicate that some orangutans appear to tell when they do not remember correct answers in memory tests.     

Orbital prefrontal cortex and guidance of instrumental behavior of rats by visuospatial stimuli predicting reward magnitude

The orbital prefrontal cortex (OPFC) is part of a circuitry mediating the perception of reward and the initiation of adaptive behavioral responses. We investigated whether the OPFC is involved in guidance of the speed of instrumental behavior by visuospatial stimuli predictive of different reward magnitudes. Unoperated rats, sham-lesioned rats, and rats with bilateral lesions of the OPFC by N-methyl-D-aspartate (NMDA) were trained in a visuospatial discrimination task. The task required a lever press on the illuminated lever of two available to obtain a food reward. Different reward magnitudes were permanently assigned to lever presses to respective sides of the operant chamber; that is, responses to one lever (e.g., the left one) were always rewarded with one pellet and responses to the other lever with five pellets. On each trial, the position of the illuminated lever was pseudorandomly determined in advance. Results revealed that OPFC lesions did not impair acquisition of the task, as the speed of conditioned responses was significantly shorter with expectancy of a high reward magnitude. In addition, during reversal, shift and reshift of lever position–reward magnitude contingencies and under extinction conditions, performance of the OPFC-lesioned and control groups did not differ. It is concluded that the OPFC in rats might not be critical for adapting behavioral responses to changes of stimulus–reward magnitude contingencies signaled by visuospatial cues.     

How brooding minds inhibit negative material: An event-related fMRI study

Depressive brooding – a passive ruminative focus on one’s problems, negative mood and their consequences – is a thinking style that places individuals at a greater risk to develop future psychopathology. In this study, we investigated whether inter-individual differences in depressive brooding are related to neural differences underlying the inhibition of a dominant response towards negative information in favor of the concurrent (positive) response. To exclude the possibility that information processes would be confounded by sustained negative mood or enhanced stress responses, a sample of thirty never-depressed healthy individuals was selected. The Cued Emotional Control Task (CECT) was used to index the ability to enhance cognitive control when encountering a negative stimulus associated with an incompatible stimulus–response mapping. Individual brooding scores were not related to behavioral performances on the CECT. On the other hand, whole brain analyses demonstrated that trait depressive brooding scores were positively associated with activation in the posterior parts of the dorsal anterior cingulate cortex (pdACC) while successfully inhibiting a response to negative relative to positive information. These findings demonstrate that brooding minds need to recruit more pdACC activation when inhibiting a dominant response towards negative information (in favor of a response towards positive), although they are performing similarly as low brooders at the behavioral level. Future research should investigate whether and how these brooding related neural adjustments in healthy volunteers are related to future psychopathology.     

Acquisition,Extinction, Recovery,and Reversal of Different Response Sequences Under Conditional Control by Nicotine in Rats

Complex voluntary behaviors occur in sequence. Eight rats were trained in an operant procedure that used nicotine and non-drug (saline) states as interoceptive cues that signaled which of two behavioral sequences led to food reward. The distal and proximal responses in the chain were always maintained on variable interval 30-sec and fixed ratio-1 schedules, respectively, and rate differences between the responses were used as the dependent variable. Extinction and reversal training was conducted. Distal response rates were significantly greater than proximal response rates during training, testing, extinction, and reversal learning. These data suggest that (a) nicotine can establish interoceptive control over different response sequences, and (b) extinction of one response sequence may be state-dependent. The clinical relevance of extinction of complex behavioral repertoires such as drug-seeking and drug-taking behavior that are evoked by specific interoceptive cues is addressed in regard to drug abuse treatment and relapse.     

Integrating rewards and cognition in the frontal cortex

Research indicates that the dorsolateral prefrontal cortex (DLPFC) contributes to working memory and executive control, whereas the ventral frontal cortex (VFC) contributes to affective and motivational processing. Few studies have examined both the functional specificity and the integration of these regions. We did so using fMRI and a verbal working memory task in which visual cues indicated whether recall performance on an upcoming trial would be linked to a monetary reward. On the basis of prior findings obtained in delayed response tasks performed by nonhuman primates, we hypothesized that (1) VFC would show an increase only in response to a cue indicating potential for a monetary reward; (2) DLPFC would show sustained activity across a delay interval for all trials, though activity in rewarded trials would be enhanced; and (3) regions engaged in speech-based rehearsal would be relatively insensitive to monetary incentive. Our hypotheses about DLPFC and rehearsal-related regions were confirmed. In VFC regions, we failed to observe statistically significant effects of reward when the cue or delay epochs of the task were examined in isolation. However, an unexpected and significant deactivation was observed in VFC during the delay epoch; furthermore, a post hoc voxelwise analysis indicated a complex interaction between (1) the cue and delay epochs of the task and (2) the reward value of the trials. The pattern of activation and deactivation across trial types suggests that VFC is sensitive to reward cues, and that portions of DLPFC and VFC may work in opposition during the delay epoch of a working memory task in order to facilitate task performance.     

Roles of nucleus accumbens and basolateral amygdala in autoshaped lever pressing

Initially-neutral cues paired with rewards are thought to acquire motivational significance, as if the incentive motivational value of the reward is transferred to the cue. Such cues may serve as secondary reinforcers to establish new learning, modulate the performance of instrumental action (Pavlovian-instrumental transfer, PIT), and be the targets of approach and other cue-directed behaviors. Here we examined the effects of lesions of the ventral striatal nucleus accumbens (ACb) and the basolateral amygdala (BLA) on the acquisition of discriminative autoshaped lever-pressing in rats. Insertion of one lever into the experimental chamber was reinforced by sucrose delivery, but insertion of another lever was not reinforced. Although sucrose was delivered independently of the rats' behavior, sham-lesioned rats rapidly came to press the reinforced but not the nonreinforced lever. Bilateral ACb lesions impaired the initial acquisition of sign-tracking but not its terminal levels. In contrast, BLA lesions produced substantial deficits in terminal levels of sign-tracking. Furthermore, whereas ACb lesions primarily affected the probability of lever press responses, BLA lesions mostly affected the rate of responding once it occurred. Finally, disconnection lesions that disrupted communication between ACb and BLA produced both sets of deficits. We suggest that ACb is important for initial acquisition of consummatory-like responses that incorporate hedonic aspects of the reward, while BLA serves to enhance such incentive salience once it is acquired.