Eveline A. Crone

Developmental changes in real life decision making: Performance on a gambling task previously shown to depend on the ventromedial prefrontal cortex

Patients with bilateral lesions of the ventromedial prefrontal cortex, when performing gambling tasks modeling real-life decision-making, opt for choices that yield high immediate gains in spite of higher future losses. Under the hypothesis that the prefrontal cortex is the last brain region to mature, it was examined whether young children would show a similar preference for immediate prospects. In Experiment 1, 4 age groups (6-9, 10-12, 13-15 and 18-25 years olds) performed 2 versions of a computerized variant of the original Iowa gambling task under 3 different feedback conditions (no feedback, global feedback, and option-specific feedback) and completed the Raven Standard Progressive Matrices as an index of inductive reasoning ability. In Experiment 2, 3 age groups (7-8, 11-12, and 15-16 year olds) performed both task versions in addition to a working memory task (Digit Span Backwards). Results showed a developmental increase in the sensitivity to future consequences, positive or negative, that could not be explained by developmental changes in working memory capacity or inductive reasoning. It was concluded that young children share with ventromedial prefrontal patients the failure to anticipate on future outcomes.

Brain Regions Mediating Flexible Rule Use during Development

During development, children improve at retrieving and using rules to guide their behavior and at flexibly switching between these rules. In this study, we used functional magnetic resonance imaging to examine the changes in brain function associated with developmental changes in flexible rule use. Three age groups (8–12, 13–17, and 18–25 years) performed a task in which they were cued to respond to target stimuli on the basis of simple task rules. Bivalent target stimuli were associated with different responses, depending on the rule, whereas univalent target stimuli were associated with fixed responses. The comparison of bivalent and univalent trials enabled the identification of regions modulated by demands on rule representation. The comparison of rule-switch and rule-repetition trials enabled the identification of regions involved in rule switching. We have used this task previously in adults and have shown that ventrolateral prefrontal cortex (VLPFC) and the (pre)-supplementary motor area (pre-SMA/SMA) have dissociable roles in task-switching, such that VLPFC is associated most closely with rule representation, and pre-SMA/SMA is associated with suppression of the previous task set (Crone et al., 2006a). Based on behavioral data in children (Crone et al., 2004), we had predicted that regions associated with task-set suppression would show mature patterns of activation earlier in development than regions associated with rule representation. Indeed, we found an adult-like pattern of activation in pre-SMA/SMA by adolescence, whereas the pattern of VLPFC activation differed among children, adolescents, and adults. These findings suggest that two components of task-switching—rule retrieval and task-set suppression—follow distinct neurodevelopmental trajectories.

Neurocognitive development of relational reasoning

Relational reasoning is an essential component of fluid intelligence, and is known to have a protracted developmental trajectory. To date, little is known about the neural changes that underlie improvements in reasoning ability over development. In this event-related functional magnetic resonance imaging (fMRI) study, children aged 8-12 and adults aged 18-25 performed a relational reasoning task adapted from Ravens Progressive Matrices. The task included three levels of relational reasoning demands: REL-0, REL-1, and REL-2. Children exhibited disproportionately lower accuracy than adults on trials that required integration of two relations (REL-2). Like adults, children engaged lateral prefrontal cortex (PFC) and parietal cortex during task performance; however, they exhibited different time courses and activation profiles, providing insight into their approach to the problems. As in prior studies, adults exhibited increased rostrolateral PFC (RLPFC) activation when relational integration was required (REL-2 > REL-1, REL-0). Children also engaged RLPFC most strongly for REL-2 problems at early stages of processing, but this differential activation relative to REL-1 trials was not sustained throughout the trial. These results suggest that the children recruited RLPFC while processing relations, but failed to use it to integrate across two relations. Relational integration is critical for solving a variety of problems, and for appreciating analogies; the current findings suggest that developmental improvements in this function rely on changes in the profile of engagement of RLPFC, as well as dorsolateral PFC and parietal cortex.

Decision-making in disinhibited adolescents and adults: insensitivity to future consequences or driven by immediate reward?

This study examined the effects of cognitive and behavioural disinhibition on real life decision-making in three different age groups (young adults, 15-16 year-olds and 12-13 year-olds). The Disinhibition-scale of Zuckermans Sensation Seeking Scale was used to differentiate between low vs. high in cognitive disinhibition and the Matching Familiar Figures Test (Kagan et al., 1964) was used to obtain an index of behavioural inhibition. All participants completed two versions of an experimental analogue of the Iowa Card Gambling Task. In the standard version rewards were placed up front and punishments were delayed and this schedule was reversed in the other version. The results showed impaired performance of cognitively disinhibited individuals but only on the standard task, not on the reversed gambling task. Performance increased with age on both tasks. Behavioural inhibition failed to influence performance on both versions of the gambling task. These findings were interpreted to suggest that (1) real-life decision-making is intact in cognitively disinhibited individuals, and (2) the age-related increase in real life decision-making cannot be attributed to developmental changes in cognitive disinhibition.

Neural correlates of developmental differences in risk estimation and feedback processing

The primary aim of this study was to compare the neural substrates of decision-making in middle-aged children and adults. To this end, we collected fMRI data while 9-12-year-olds and 18-26-year-olds performed a simple gambling task. The task was designed to tap two important aspects of decision-making: risk estimation and feedback processing. We examined how orbitofrontal cortex (OFC), anterior cingulate cortex (ACC), and dorsolateral prefrontal cortex (DLPFC) contributed to risk estimation, and how ventrolateral and medial prefrontal cortices (VLPFC and medial PFC) contributed to negative feedback processing in children and adults. Region of interest analyses revealed differences in brain activation between children and adults for ACC and lateral OFC. ACC was recruited more for high-risk than for low-risk trials, and this difference was larger for children than for adults. In contrast, children and adults did not differ in activation for OFC or DLPFC. These data suggest that childrens decision-making under uncertainty is associated with a high degree of response conflict. Both age groups exhibited bilateral VLPFC (BA 47) and medial PFC/ACC (BA 6/ BA 32 (dorsal) and 24 (ventral)) activation associated with negative feedback processing. Relative to adults, children engaged lateral OFC more strongly for negative relative to positive feedback. These results indicate that children may find negative feedback more aversive than adults do. In summary, children aged 9-12 years and adults recruit similar brain regions during risk-estimation and feedback processing, but some key differences between the groups provide insight into the factors contributing to developmental changes in decision-making.

Characterization of children's decision making: Sensitivity to punishment frequency, not task complexity

On a gambling task that models real-life decision making, children between ages 7 and 12 perform like patients with bilateral lesions of the ventromedial prefrontal cortex (VMPFC), opting for choices that yield high immediate gains in spite of higher future losses (Crone & Van der Molen, 2004). The current study set out to characterize developmental changes in decision making by varying task complexity and punishment frequency. Three age groups (7–9 years, 10–12 years, 13–15 years) performed two versions of a computerized variant of the original Iowa gambling task. Task complexity was manipulated by varying the number of choices participants could make. Punishment frequency was manipulated by varying the frequency of delayed punishment. Results showed a developmental increase in the sensitivity to future consequences, which was present only when the punishment was presented infrequently. These results could not be explained by differential sensitivity to task complexity, hypersensitivity to reward, or failure to switch response set after receiving punishment. There was a general pattern of boys outperforming girls by making more advantageous choices over the course of the task. In conclusion, 7–12-year-old children—like VMPFC patients—appear myopic about the future except when the potential for future punishment is high.

Changing Brains, Changing Perspectives The Neurocognitive Development of Reciprocity

Adolescence is characterized by the emergence of advanced forms of social perspective taking and significant changes in social behavior. Yet little is known about how changes in social cognition are related to changes in brain function during adolescence. In this study, we investigated the neural correlates of social behavior during three phases of adolescence, carrying out functional magnetic resonance imaging of participants’ brains while they were Player 2 in the Trust Game. We found that with age, adolescents were increasingly sensitive to the perspective of the other player, as indicated by their reciprocal behavior. These advanced forms of social perspective-taking behavior were associated with increased involvement of the left temporo-parietal junction and the right dorsolateral prefrontal cortex. In contrast, young adolescents showed more activity in the anterior medial prefrontal cortex, a region previously associated with self-oriented processing and mentalizing. These findings suggest that the asynchronous development of these neural systems may underlie the shift from thinking about self to thinking about the other.

Striatum–Medial Prefrontal Cortex Connectivity Predicts Developmental Changes in Reinforcement Learning

During development, children improve in learning from feedback to adapt their behavior. However, it is still unclear which neural mechanisms might underlie these developmental changes. In the current study, we used a reinforcement learning model to investigate neurodevelopmental changes in the representation and processing of learning signals. Sixty-seven healthy volunteers between ages 8 and 22 (children: 8-11 years, adolescents: 13-16 years, and adults: 18-22 years) performed a probabilistic learning task while in a magnetic resonance imaging scanner. The behavioral data demonstrated age differences in learning parameters with a stronger impact of negative feedback on expected value in children. Imaging data revealed that the neural representation of prediction errors was similar across age groups, but functional connectivity between the ventral striatum and the medial prefrontal cortex changed as a function of age. Furthermore, the connectivity strength predicted the tendency to alter expectations after receiving negative feedback. These findings suggest that the underlying mechanisms of developmental changes in learning are not related to differences in the neural representation of learning signals per se but rather in how learning signals are used to guide behavior and expectations.

Sensitivity to interference and response contingencies in attention-deficit/hyperactivity disorder.

BACKGROUNDnCurrent theories on ADHD suggest executive and motivational deficits, but it remains unclear whether these are separate deficits or a unitary deficit.nnnMETHODnADHD children and matched controls performed on a hybrid disjunctive-choice reaction time task in which target stimuli could be surrounded by flankers signaling either the appropriate response, the competing response, or response inhibition. The task was performed under three conditions; reward only, reward and occasional punishment, and equal probability of reward and punishment. Heart rate and skin conductance measures were taken during task performance.nnnRESULTSnContrary to control children, ADHD children slowed their responses when flankers cueing the appropriate response surrounded the stimulus. Flankers cueing incorrect responses further slowed ADHD children relative to control children. ADHD children also responded less accurately under the threat of punishment. Phasic heart rate did not differ between groups, but immediate reward feedback induced greater heart rate responses in control than in ADHD children. Contrary to expectations, groups did not differ in skin conductance responses.nnnCONCLUSIONSnADHD children appear deficient in approach tendencies in the presence of imminent reward, rather than unresponsive to punishment or negative feedback. Executive inhibition and motivational inhibition seemed to exert separate effects on behavior of children with ADHD.

Neural Circuitry Underlying Rule Use in Humans and Nonhuman Primates

Much of our behavior is focused on minimizing or maximizing a particular goal state. For example, animals generally seek to maximize food intake and minimize energy expenditure ([Stephens and Krebs, 1986][1]), although some humans strive to achieve the exact opposite goals. Instrumental to goal-