The study examined the relationship between risk-taking behavior during selection of monetary rewards and activations in the anterior cingulate cortex (ACC), orbitofrontal cortex (OFC) and medial prefrontal cortex (mPFC), brain regions that are associated with decision-making. Thirty-three adolescents with no personal or family history of any psychiatric illness were administered the Wheel of Fortune (WOF) task using a functional magnetic resonance imaging protocol. The WOF is a computerized two-choice, probabilistic monetary reward task. Selection of a reward, particularly a low-probability/high-magnitude reward choice, induced greater activations in dorsal ACC, ventrolateral OFC and mPFC than the control condition. Although similar findings have been reported by earlier studies, the results from this study were not impacted by reaction times and expected values and persisted even after controlling for sociodemographic factors. Post-hoc analysis revealed greater activation of ACC and mPFC in response to selection of rewards of larger magnitude than those of smaller magnitude when the probability of reward was maintained constant. Adolescents with greater frequency of high-risk behavior (defined as low-probability/high magnitude reward choice) had lower activation of ACC, OFC and mPFC than those who engaged in this behavior less frequently. These findings suggest individual differences in prefrontal cortical function with regards to decision-making process in adolescents.
Neurobiology; choice; selection; adolescents; decision-making; rewards
Functional magnetic resonance imaging (fMRI) was used to measure activity in three frontal cortical areas, lateral orbitofrontal cortex (lOFC), medial orbitofrontal cortex/ventromedial frontal cortex (mOFC/vmPFC), and anterior cingulate cortex (ACC) when expectations about type of reward, and not just reward presence or absence, could be learned. Two groups of human subjects learned twelve stimulus-response pairings. In one group (Consistent), correct performances of a given pairing were always reinforced with a specific reward outcome whereas in the other group (Inconsistent), correct performances were reinforced with randomly selected rewards. MOFC/vmPFC and lOFC were not distinguished by simple differences in relative preference for positive and negative outcomes. Instead lOFC activity reflected updating of reward-related associations specific to reward type; lOFC was active whenever informative outcomes allowed updating of reward-related associations regardless of whether the outcomes were positive or negative and the effects were greater when consistent stimulus-outcome and response-outcome mappings were present. A psycho-physiological interaction (PPI) analysis demonstrated changed coupling between lOFC and brain areas for visual object representation, such as perirhinal cortex, and reward-guided learning, such as amygdala, ventral striatum, and habenula /mediodorsal thalamus. By contrast mOFC/vmPFC activity reflected expected values of outcomes and occurrence of positive outcomes, irrespective of consistency of outcome mappings. The third frontal cortical region, ACC, reflected the use of reward type information to guide response selection. ACC activity reflected the probability of selecting the correct response, was greater when consistent outcome mappings were present, and was related to individual differences in propensity to select the correct response.
Positive behavioral responses to attractive faces have led neuroscientists to investigate underlying neural mechanisms in a ‘reward circuit’ that includes brain regions innervated by dopamine pathways. Using male faces ranging from attractive to extremely unattractive, disfigured ones, this study is the first to demonstrate heightened responses to both rewarding and aversive faces in numerous areas of this putative reward circuit. Parametric analyses employing orthogonal linear and nonlinear regressors revealed positive nonlinear effects in anterior cingulate cortex (ACC), lateral orbitofrontal cortex (LOFC), striatum (nucleus accumbens (NAC), caudate, putamen), and ventral tegmental area (VTA), in addition to replicating previously documented linear effects in MOFC and LOFC and nonlinear effects in AMY and MOFC. The widespread nonlinear responses are consistent both with single cell recordings in animals showing responses to both rewarding and aversive stimuli and some human fMRI investigations of non-face stimuli. They indicate that the reward circuit does not process face valence with any simple dissociation of function across structures. Perceiver gender modulated some responses to our male faces: women showed stronger linear effects, and men showed stronger nonlinear effects, which may have functional implications. Our discovery of nonlinear responses to attractiveness throughout the reward circuit echoes the history of amygdala research: early work indicated a linear response to threatening stimuli, including faces; later work also revealed a nonlinear response with heightened activation to affectively salient stimuli regardless of valence. The challenge remains to determine how such dual coding influences feelings, like pleasure and pain, and guides goal-related behavioral responses, like approach and avoidance.
facial attractiveness; fMRI; reward circuit
This study examined whether ventral frontostriatal regions differentially code expected and unexpected reward outcomes. We parametrically manipulated the probability of reward and examined the neural response to reward and nonreward for each probability condition in the ventral striatum and the orbitofrontal cortex (OFC). By late trials of the experiment, subjects showed slower behavioral responses for the condition with the lowest probability of reward, relative to the condition with the highest probability of reward. At the neural level, both the nucleus accumbens (NAcc) and OFC showed greater activation to rewarded relative to nonrewarded trials, but the accumbens appeared to be most sensitive to violations in expected reward outcomes. These data suggest distinct roles for frontostriatal circuitry in reward prediction and in responding to violations in expectations.
Anhedonia, the reduced propensity to experience pleasure, is a promising endophenotype and vulnerability factor for several psychiatric disorders, including depression and schizophrenia. In the present study, we used resting electroencephalograms, functional magnetic resonance imaging, and volumetric analyses to probe putative associations between anhedonia and individual differences in key nodes of the brain’s reward system in a non-clinical sample. We found that anhedonia, but not other symptoms of depression or anxiety, was correlated with reduced nucleus accumbens (NAcc) responses to rewards (gains in a monetary incentive delay task), reduced NAcc volume, and increased resting delta current density (i.e., decreased resting activity) in the rostral anterior cingulate cortex (rACC), an area previously implicated in positive subjective experience. In addition, NAcc reward responses were inversely associated with rACC resting delta activity, supporting the hypothesis that delta might be lawfully related to activity within the brain’s reward circuit. Taken together, these results help elucidate the neural basis of anhedonia and strengthen the argument for anhedonia as an endophenotype for depression.
depression; anhedonia; striatum; reward; anterior cingulate cortex
Stimulant dependence is associated with neuropsychological impairments. Here, we summarize and integrate the existing neuroimaging literature on the neural substrates of neuropsychological (dys)function in stimulant dependence, including cocaine, (meth-)amphetamine, ecstasy and nicotine dependence, and excessive caffeine use, comparing stimulant abusers (SAs) to nondrug using healthy controls (HCs). Despite some inconsistencies, most studies indicated altered brain activation in prefrontal cortex (PFC) and insula in response to reward and punishment, and higher limbic and anterior cingulate cortex (ACC)/PFC activation during craving and attentional bias paradigms in SAs compared with HCs. Impulsivity in SAs was associated with lower ACC and presupplementary motor area activity compared with HCs, and related to both ventral (amygdala, ventrolateral PFC, insula) and dorsal (dorsolateral PFC, dorsal ACC, posterior parietal cortex) systems. Decision making in SAs was associated with low dorsolateral PFC activity and high orbitofrontal activity. Finally, executive function in SAs was associated with lower activation in frontotemporal regions and higher activation in premotor cortex compared with HCs. It is concluded that the lower activations compared with HCs are likely to reflect the neural substrate of impaired neurocognitive functions, whereas higher activations in SAs compared with HCs are likely to reflect compensatory cognitive control mechanisms to keep behavioral task performance to a similar level as in HCs. However, before final conclusions can be drawn, additional research is needed using neuroimaging in SAs and HCs using larger and more homogeneous samples as well as more comparable task paradigms, study designs, and statistical analyses.
Addiction; fMRI; functional imaging; magnetic resonance imaging; stimulant dependence; stimulants
Social decisions play a crucial role in the success of individuals and the groups they compose. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders like autism and sociopathy. We studied how neurons in three frontal cortical areas encode the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, reward allocations to oneself, or both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or no one. Within this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerges as a key nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.
Damage to prefrontal cortex (PFC) impairs decision-making, but the underlying value computations that might cause such impairments remain unclear. Here we report that value computations are doubly dissociable within PFC neurons. While many PFC neurons encoded chosen value, they used opponent encoding schemes such that averaging the neuronal population eliminated value coding. However, a special population of neurons in anterior cingulate cortex (ACC) - but not orbitofrontal cortex (OFC) - multiplex chosen value across decision parameters using a unified encoding scheme, and encoded reward prediction errors. In contrast, neurons in OFC - but not ACC - encoded chosen value relative to the recent history of choice values. Together, these results suggest complementary valuation processes across PFC areas: OFC neurons dynamically evaluate current choices relative to recent choice values, while ACC neurons encode choice predictions and prediction errors using a common valuation currency reflecting the integration of multiple decision parameters.
Vulnerability to drug abuse is related to both reward seeking and impulsivity, two constructs thought to have a biological basis in the prefrontal cortex (PFC). This review addresses similarities and differences in neuroanatomy, neurochemistry and behavior associated with PFC function in rodents and primates. Emphasis is placed on monoamine and amino acid neurotransmitter systems located in anatomically distinct subregions: medial prefrontal cortex (mPFC); lateral prefrontal cortex (lPFC); anterior cingulate cortex (ACC); and orbitofrontal cortex (OFC). While there are complex interconnections and overlapping functions among these regions, each is thought to be involved in various functions related to health-related risk behaviors and drug abuse vulnerability. Among the various functions implicated, evidence suggests that mPFC is involved in reward processing, attention and drug reinstatement; lPFC is involved in decision-making, behavioral inhibition and attentional gating; ACC is involved in attention, emotional processing and self-monitoring; and OFC is involved in behavioral inhibition, signaling of expected outcomes and reward/punishment sensitivity. Individual differences factors (e.g., age and sex) influence functioning of these regions, which, in turn, impacts drug abuse vulnerability. Implications for the development of drug abuse prevention and treatment strategies aimed at engaging PFC inhibitory processes that may reduce risk-related behaviors are discussed, including the design of effective public service announcements, cognitive exercises, physical activity, direct current stimulation, feedback control training and pharmacotherapies. A major challenge in drug abuse prevention and treatment rests with improving intervention strategies aimed at strengthening PFC inhibitory systems among at-risk individuals.
Anterior cingulate cortex; Dopamine; Drug abuse; GABA; Glutamate; Impulsivity; Lateral prefrontal cortex; Medial prefrontal cortex; Norepinephrine; Orbitofrontal cortex; Serotonin
Neuroimaging studies of obsessive-compulsive disorder have found abnormalities in orbitofronto-striato-thalamic circuitry, including the orbitofrontal cortex, anterior cingulate cortex, caudate, and thalamus, but few studies have explored abnormal intrinsic or spontaneous brain activity in the resting state. We investigated both intra- and inter-regional synchronized activity in twenty patients with obsessive-compulsive disorder and 20 healthy controls using resting-state functional magnetic resonance imaging. Regional homogeneity (ReHo) and functional connectivity methods were used to analyze the intra- and inter-regional synchronized activity, respectively. Compared with healthy controls, patients with obsessive-compulsive disorder showed significantly increased ReHo in the orbitofrontal cortex, cerebellum, and insula, and decreased ReHo in the ventral anterior cingulate cortex, caudate, and inferior occipital cortex. Based on ReHo results, we determined functional connectivity differences between the orbitofrontal cortex and other brain regions in both patients with obsessive-compulsive disorder and controls. We found abnormal functional connectivity between the orbitofrontal cortex and ventral anterior cingulate cortex in patients with obsessive-compulsive disorder compared with healthy controls. Moreover, ReHo in the orbitofrontal cortex was correlated with the duration of obsessive-compulsive disorder. These findings suggest that increased intra- and inter-regional synchronized activity in the orbitofrontal cortex may have a key role in the pathology of obsessive-compulsive disorder. In addition to orbitofronto-striato-thalamic circuitry, brain regions such as the insula and cerebellum may also be involved in the pathophysiology of obsessive-compulsive disorder.
The development of reward-based learning and decision-making, and the neural circuitry underlying these processes, appears to be influenced negatively by adverse child-rearing environments characterized by abuse and other forms of maltreatment. No research to-date has investigated whether normative variations in the child-rearing environment have effects on adolescent brain structure. We examined whether normative variations in maternal responses to adolescents’ positive affective behavior were associated with morphometric measures of the adolescents’ affective neural circuitry, namely the amygdala, orbitofrontal cortex (OFC), and anterior cingulate cortex (ACC). Healthy adolescents (N = 113) participated in laboratory-based interaction tasks with their mothers, and underwent high-resolution (3T) structural magnetic resonance imaging (MRI). The mother–adolescent interactions included a pleasant event-planning interaction (EPI) and a conflictual problem-solving interaction (PSI). Adolescents, whose mothers displayed more punishing responses to their positive affective behavior during both tasks, and only during the PSI, had larger left dorsal ACC and bilateral OFC volumes, respectively. In addition, boys whose mothers evidenced this pattern of behavior during the EPI had larger right amygdala volumes. These results suggest that normative variations in maternal responses to affective behavior are associated with the structural characteristics of adolescents’ affective neural circuitry, which may have implications for the development of their social, cognitive and affective functioning.
reward; neuroimaging; family; parenting; brain structure
Deep brain stimulation (DBS) has emerged as a safe, effective, and reversible treatment for a number of movement disorders. This has prompted investigation of its use for other applications including psychiatric disorders. In recent years, DBS has been introduced for the treatment of obsessive compulsive disorder (OCD), which is characterized by recurrent unwanted thoughts or ideas (obsessions) and repetitive behaviors or mental acts performed in order to relieve these obsessions (compulsions). Abnormal activity in cortico-striato-thalamo-cortical (CSTC) circuits including the orbitofrontal cortex (OFC), anterior cingulate cortex (ACC), ventral striatum, and mediodorsal (MD) thalamus has been implicated in OCD. To this end a number of DBS targets including the anterior limb of the internal capsule (ALIC), ventral capsule/ventral striatum (VC/VS), ventral caudate nucleus, subthalamic nucleus (STN), and nucleus accumbens (NAc) have been investigated for the treatment of OCD. Despite its efficacy and widespread use in movement disorders, the mechanism of DBS is not fully understood, especially as it relates to psychiatric disorders. While initially thought to create a functional lesion akin to ablative procedures, it is increasingly clear that DBS may induce clinical benefit through activation of axonal fibers spanning the CSTC circuits, alteration of oscillatory activity within this network, and/or release of critical neurotransmitters. In this article we review how the use of DBS for OCD informs our understanding of both the mechanisms of DBS and the circuitry of OCD. We review the literature on DBS for OCD and discuss potential mechanisms of action at the neuronal level as well as the broader circuit level.
deep brain stimulation; obsessive compulsive disorder; neuromodulation; cortico-striato-thalamocortical circuit
To optimally obtain desirable outcomes, organisms must track outcomes predicted by stimuli in the environment (stimulus-outcome or SO associations) and outcomes predicted by their own actions (action-outcome or AO associations). Anterior cingulate cortex (ACC) and orbitofrontal cortex (OFC) are implicated in tracking outcomes, but anatomical and functional studies suggest a dissociation, with ACC and OFC responsible for encoding AO and SO associations, respectively. To examine whether this dissociation held at the single neuron level, we trained two subjects to perform choice tasks that required using AO or SO associations. OFC and ACC neurons encoded the action that the subject used to indicate its choice, but this encoding was stronger in OFC during the SO task and stronger in ACC during the AO task. These results are consistent with a division of labor between the two areas in terms of using rewards associated with either stimuli or actions to guide decision-making.
Stress and alcohol context cues are each associated with alcohol-related behaviors, yet neural responses underlying these processes remain unclear. The present study investigated the neural correlates of stress and alcohol context cue experiences and examined sex differences in these responses. Using functional magnetic resonance imaging, brain responses were examined while 43 right-handed, socially drinking, healthy individuals (23 females) engaged in brief guided imagery of personalized stress, alcohol-cue and neutral-relaxing scenarios. Stress and alcohol-cue exposure increased activity in the cortico-limbic-striatal circuit (p<.01, corrected), encompassing the medial prefrontal cortex (mPFC), orbitofrontal cortex (OFC), anterior cingulate cortex (ACC), left anterior insula, striatum and visuomotor regions (parietal and occipital lobe, and cerebellum). Activity in the right dorsal striatum increased during stress, while bilateral ventral striatum activity was evident during alcohol-cue exposure. Men displayed greater stress-related activations in the mPFC, rostral ACC, posterior insula, amygdala and hippocampus than women, whereas women showed greater alcohol-cue related activity in the superior and middle frontal gyrus (SFG/MFG) than men. Stress-induced anxiety was positively associated with activity in emotion modulation regions, including the medial OFC, ventromedial PFC, left superior-medial PFC and rostral ACC in men, but in women with activation in the SFG/MFG, regions involved in cognitive processing. Alcohol craving was significantly associated with the striatum (encompassing dorsal and ventral) in men, supporting its involvement in alcohol ‘urge’ in healthy men. These results indicate sex differences in neural processing of stress and alcohol-cue experiences, and have implications for sex-specific vulnerabilities to stress- and alcohol-related psychiatric disorders.
Sex differences; Stress; Alcohol cue; Reward; Brain fMRI; Prefrontal Cortex
Cognition can influence emotion by biasing neural activity in the first cortical region in which the reward value and subjective pleasantness of stimuli is made explicit in the representation, the orbitofrontal cortex (OFC). The same effect occurs in a second cortical tier for emotion, the anterior cingulate cortex (ACC). Similar effects are found for selective attention, to for example the pleasantness vs. the intensity of stimuli, which modulates representations of reward value and affect in the orbitofrontal and anterior cingulate cortices. The mechanisms for the effects of cognition and attention on emotion are top-down biased competition and top-down biased activation. Affective and mood states can in turn influence memory and perception, by backprojected biasing influences. Emotion-related decision systems operate to choose between gene-specified rewards such as taste, touch, and beauty. Reasoning processes capable of planning ahead with multiple steps held in working memory in the explicit system can allow the gene-specified rewards not to be selected, or to be deferred. The stochastic, noisy, dynamics of decision-making systems in the brain may influence whether decisions are made by the selfish-gene-specified reward emotion system, or by the cognitive reasoning system that explicitly calculates reward values that are in the interests of the individual, the phenotype.
cognition; emotion; orbitofrontal cortex; decision-making; the noisy brain; planning
The attribution of personal relevance, i.e. relating internal and external stimuli to establish a sense of belonging, is a common phenomenon in daily life. Although previous research demonstrated a relationship between reward and personal relevance, their exact neuronal relationship including the impact of personality traits remains unclear.
Using functional magnetic resonance imaging, we applied an experimental paradigm that allowed us to explore the neural response evoked by reward and the attribution of personal relevance separately. We observed different brain regions previously reported to be active during reward and personal relevance, including the bilateral caudate nucleus and the pregenual anterior cingulate cortex (PACC). Additional analysis revealed activations in the right and left insula specific for the attribution of personal relevance. Furthermore, our results demonstrate a negative correlation between signal changes in both the PACC and the left anterior insula during the attribution of low personal relevance and the personality dimension novelty seeking.
While a set of subcortical and cortical regions including the PACC is commonly involved in reward and personal relevance, other regions like the bilateral anterior insula were recruited specifically during personal relevance. Based on our correlation between novelty seeking and signal changes in both regions during personal relevance, we assume that the neuronal response to personally relevant stimuli is dependent on the personality trait novelty seeking.
Nicotine is the principle addictive agent delivered via cigarette smoking. The addictive activity of nicotine is due to potent interactions with nicotinic acetylcholine receptors (nAChRs) on neurons in the reinforcement and reward circuits of the brain. Beyond its addictive actions, nicotine is thought to have positive effects on performance in working memory and short-term attention-related tasks. The brain areas involved in such behaviors are part of an extensive cortico-limbic network that includes relays between prefrontal cortex (PFC) and cingulate cortex (CC), hippocampus, amygdala, ventral tegmental area (VTA) and the nucleus accumbens (nAcc). Nicotine activates a broad array of nAChRs subtypes that can be targeted to pre- as well as peri- and post-synaptic locations in these areas. Thereby, nicotine not only excites different types of neurons, but it also perturbs baseline neuronal communication, alters synaptic properties and modulates synaptic plasticity.
In this review we focus on recent findings on nicotinic modulation of cortical circuits and their targets fields, which show that acute and transient activation of nicotinic receptors in cortico-limbic circuits triggers a series of events that affects cognitive performance in a long lasting manner. Understanding how nicotine induces long-term changes in synapses and alters plasticity in the cortico-limbic circuits is essential to determining how these areas interact in decoding fundamental aspects of cognition and reward.
Nicotine; Cognition; Limbic; Acetylcholine; Synaptic plasticity
Although the lesions of patients with impaired social behaviour encompass both orbitofrontal and anterior cingulate cortex (OFC and ACC), attempts to model such impairments in animals have focused on the OFC. However, recent neuroimaging attempts to identify the neural correlates of social interaction have emphasized the relative importance of ACC. Here we report the effect of circumscribed excitotoxic lesions of either OFC or ACC on ethological, unconditioned tests of emotion and social behaviour in the Lister hooded rat. OFC lesions altered emotional responsiveness to stimuli in non-social, fear-inducing situations (hyponeophagia test), and produced a small but statistically significant increase in aggression to other rats, but did not compromise other aspects of social interaction and appraisal. ACC lesions did, however, affect the utilization of social information. Specifically, ACC lesions diminished interest in other individuals and caused a relative reduction in memory for social stimuli. Whereas normal animals habituated to repeated presentations of the same individual, the poor performance of ACC animals entailed continued higher levels of responsiveness to repeated presentations of the same individual. The ACC impairment cannot simply be attributed to a general reduction in arousal, or a general impairment in recognition memory. Neither lesion affected anxiety per se (successive alleys test). Further analyses were conducted to investigate whether the changes in aggressive and social behaviour were related to different aspects of decision-making. Although the relationship between changes in social interaction and decision-making after ACC lesions is unclear, OFC impairments in emotionality were correlated with increased impulsive choice.
anxiety; behaviour; emotion; rat
This study examined the functional specificity of dorsal anterior cingulate cortex (dACC) and medial prefrontal cortex (mPFC) regarding two elements of decision-making: the number of available decision options and the level of expected reward. Eighteen healthy participants were trained to recognize the reward value associated with several visual stimuli, and then were presented with groups of two, three, or four of these stimuli and asked to select the object associated with the highest reward. BOLD activation in dorsomedial prefrontal cortex (dmFC)/dACC was strongly positively associated with increases in the number of decision options but only weakly associated with increases in the level of expected reward. Activation in rostral anterior cingulate cortex (rACC)/mPFC and amygdala was related to increases in the level of expected reward but not increases in the number of decision options. The current results suggest functional specificity with respect to the roles of dACC/dmFC and rACC/mPFC in decision-making.
decision; FMRI; anterior cingulate; caudate; medial prefrontal cortex; amygdala
Little is known about brain mechanisms supporting the experience of chronic puritus in disease states.
To examine the difference in brain processing of histamine-induced itch in patients with active atopic dermatitis (AD) vs. healthy controls with the emerging technique of functional magnetic resonance imaging (fMRI) using arterial spin labelling (ASL).
Itch was induced with histamine iontophoresis in eight patients with AD and seven healthy subjects.
We found significant differences in brain processing of histamine-induced itch between patients with AD and healthy subjects. Patients with AD exhibited bilateral activation of the anterior cingulate cortex (ACC), posterior cingulate cortex (PCC), retrosplenial cingulate cortex and dorsolateral prefrontal cortex (DLPFC) as well as contralateral activation of the caudate nucleus and putamen. In contrast, healthy subjects activated the primary motor cortex, primary somatosensory cortex and superior parietal lobe. The PCC and precuneus exhibited significantly greater activity in patients vs. healthy subjects. A significant correlation between percentage changes of brain activation was noted in the activation of the ACC and contralateral insula and histamine-induced itch intensity as well as disease severity in patients with AD. In addition, an association was noted between DLPFC activity and disease severity.
Our results demonstrate that ASL fMRI is a promising technique to assess brain activity in chronic itch. Brain activity of acute itch in AD seems to differ from that in healthy subjects. Moreover, the activity in cortical areas involved in affect and emotion correlated to measures of disease severity.
anterior cingulate cortex; arterial spin labelling; atopic dermatitis; functional magnetic resonance imaging; histamine; pruritus
A heightened propensity for risk-taking and poor decision-making underlies the peak morbidity and mortality rates reported during adolescence. Delayed maturation of cortical structures during the adolescent years has been proposed as a possible explanation for this observation. Here, we test the hypothesis of adolescent delayed maturation by using fMRI during a monetary decision-making task that directly examines risk-taking behavior during choice selection. Orbitofrontal/ventrolateral prefrontal cortex (OFC/VLPFC) and dorsal anterior cingulate cortex (ACC) were examined selectively since both have been implicated in reward-related processes, cognitive control, and resolution of conflicting decisions. Group comparisons revealed greater activation in the OFC/VLPFC (BA 47) and dorsal ACC (BA 32) in adults than adolescents when making risky selections. Furthermore, reduced activity in these areas correlated with greater risk-taking performance in adolescents and in the combined group. Consistent with predictions, these results suggest that adolescents engage prefrontal regulatory structures to a lesser extent than adults when making risky economic choices.
reward; decision-making; cognitive control; affective regulation; conflict monitoring
How does the brain translate information signaling potential rewards into motivation to get them? Motivation to obtain reward is thought to depend on the midbrain, (particularly the ventral tegmental area, VTA), the nucleus accumbens (NAcc), and the dorsolateral prefrontal cortex (dlPFC), but it is not clear how the interactions amongst these regions relate to reward-motivated behavior. To study the influence of motivation on these reward-responsive regions and on their interactions, we used Dynamic Causal Modeling (DCM) to analyze functional magnetic resonance imaging (fMRI) data from humans performing a simple task designed to isolate reward anticipation. The use of fMRI permitted the simultaneous measurement of multiple brain regions while human participants anticipated and prepared for opportunities to obtain reward, thus allowing characterization of how information about reward changes physiology underlying motivational drive. Further, we modeled the impact of external reward cues on causal relationships within this network, thus elaborating a link between physiology, connectivity, and motivation. Specifically, our results indicated that dlPFC was the exclusive entry point of information about reward in this network, and that anticipated reward availability caused VTA activation only via its effect on the dlPFC. Anticipated reward thus increased dlPFC activation directly, whereas it influenced VTA and NAcc only indirectly, by enhancing intrinsically weak or inactive pathways from the dlPFC. Our findings of a directional prefrontal influence on dopaminergic regions during reward anticipation suggest a model in which the dlPFC integrates and transmits representations of reward to the mesolimbic and mesocortical dopamine systems, thereby initiating motivated behavior.
We investigated adolescent brain processing of decisions under conditions of varying risk, reward, and uncertainty. Adolescents (n = 31) preformed a Decision–Reward Uncertainty task that separates decision uncertainty into behavioral and reward risk, while they were scanned using functional magnetic resonance imaging. Behavioral risk trials involved uncertainty about which action to perform to earn a fixed monetary reward. In contrast, during reward risk the decision that might lead to a reward was known, but the likelihood of earning a reward was probabilistically determined. Behavioral risk trials evoked greater activation than the reward risk and no risk conditions in the anterior cingulate, medial frontal gyrus, bilateral frontal poles, bilateral inferior parietal lobe, precuneus, bilateral superior-middle frontal gyrus, inferior frontal gyrus, and insula. Our results were similar to those of young adults using the same task (Huettel, 2006) except that adolescents did not show significant activation in the posterior supramarginal gyrus during behavioral risk. During the behavioral risk condition regardless of reward outcome, overall mean frontal pole activity showed a positive correlation with age during the behavioral and reward risk conditions suggesting a developmental difference of this region of interest. Additionally, reward response to the Decision–Reward Uncertainty task in adolescents was similar to that seen in young adults (Huettel, 2006). Our data did not show a correlation between age and mean ventral striatum activity during the three conditions. While our results came from a healthy high functioning non-maltreated sample of adolescents, this method can be used to address types of risks and reward processing in children and adolescents with predisposing vulnerabilities and add to the paucity of imaging studies of risk and reward processing during adolescence.
risk; behavioral risk; decision making; reward; adolescence; prefrontal brain regions; reward response; nucleus accumbens
We investigated how different sub-regions of rodent prefrontal cortex contribute to value-based decision making, by comparing neural signals related to animal’s choice, its outcome, and action value in orbitofrontal cortex (OFC) and medial prefrontal cortex (mPFC) of rats performing a dynamic two-armed bandit task. Neural signals for upcoming action selection arose in the mPFC, including the anterior cingulate cortex, only immediately before the behavioral manifestation of animal’s choice, suggesting that rodent prefrontal cortex is not involved in advanced action planning. Both OFC and mPFC conveyed signals related to the animal’s past choices and their outcomes over multiple trials, but neural signals for chosen value and reward prediction error were more prevalent in the OFC. Our results suggest that rodent OFC and mPFC serve distinct roles in value-based decision making, and that the OFC plays a prominent role in updating the values of outcomes expected from chosen actions.
In dynamic environments, adaptive behavior requires striking a balance between harvesting currently available rewards (exploitation) and gathering information about alternative options (exploration) [1–4]. Such strategic decisions should incorporate not only recent reward history, but also opportunity costs and environmental statistics. Previous neuroimaging [5–8] and neurophysiological [9–13] studies have implicated several brain areas, including orbitofrontal cortex, anterior cingulate cortex, and ventral striatum, in distinguishing between bouts of exploration and exploitation. Nonetheless, the neuronal mechanisms that underlie selection between these strategies remain poorly understood. We hypothesized that posterior cingulate cortex (CGp), an area linking reward processing, attention , memory [15, 16], and motor control systems , mediates the integration of decision variables such as reward , uncertainty , and target location  that underlie the dynamic balance of exploration and exploitation. Here we show that CGp neurons distinguish between exploratory and exploitative decisions made by monkeys in a dynamic foraging task. Moreover, the firing rates of these neurons predict in graded fashion the strategy most likely to be selected on upcoming trials. This encoding is distinct from mere switching between spatial targets, and is independent of the absolute magnitudes of rewards. These observations implicate CGp in both the integration of individual outcomes across decision making and the modification of strategy in dynamic environments.