Koji Jimura

Analyses of regional-average activation and multivoxel pattern information tell complementary stories

Multivariate pattern analysis (MVPA) has recently received increasing attention in functional neuroimaging due to its ability to decode mental states from fMRI signals. However, questions remain regarding both the empirical and conceptual relationships between results from MVPA and standard univariate analyses. In the current study, whole-brain univariate and searchlight MVPAs of parametric manipulations of monetary gain and loss in a decision making task (Tom et al., 2007) were compared to identify the differences in the results across these methods and the implications for understanding the underlying mental processes. The MVPA and univariate results did identify some overlapping regions in whole brain analyses. However, an analysis of consistency revealed that in many regions the effect size estimates obtained from MVPA and univariate analysis were uncorrelated. Moreover, comparison of sensitivity showed a general trend towards greater sensitivity to task manipulations by MVPA compared to univariate analysis. These results demonstrate that MVPA methods may provide a different view of the functional organization of mental processing compared to univariate analysis, wherein MVPA is more sensitive to distributed coding of information whereas univariate analysis is more sensitive to global engagement in ongoing tasks. The results also highlight the need for better ways to integrate these methods.

Domain independence and stability in young and older adults' discounting of delayed rewards

Individual discounting rates for different types of delayed reward are typically assumed to reflect a single, underlying trait of impulsivity. Recently, we showed that discounting rates are orders of magnitude steeper for directly consumable liquid rewards than for monetary rewards (Jimura et al., 2009), raising the question of whether discounting rates for different types of reward covary at the individual level. Accordingly, the present study examined the relation between discounting of hypothetical money and real liquid rewards in young adults (Experiment 1) and older adults (Experiment 2). At the group level, young adults discounted monetary rewards more steeply than the older adults, but there was no significant age difference with respect to liquid rewards. At the individual level, the rates at which young and older participants discounted each reward type were stable over a two- to fifteen-week interval (rs>70), but there was no significant correlation between the rates at which they discounted the two reward types. These results suggest that although similar decision-making processes may underlie the discounting of different types of rewards, the rates at which individuals discount money and directly consumable rewards may reflect separate, stable traits, rather than a single trait of impulsivity.

Primary and Secondary Rewards Differentially Modulate Neural Activity Dynamics during Working Memory

Background Cognitive control and working memory processes have been found to be influenced by changes in motivational state. Nevertheless, the impact of different motivational variables on behavior and brain activity remains unclear. Methodology/Principal Findings The current study examined the impact of incentive category by varying on a within-subjects basis whether performance during a working memory task was reinforced with either secondary (monetary) or primary (liquid) rewards. The temporal dynamics of motivation-cognition interactions were investigated by employing an experimental design that enabled isolation of sustained and transient effects. Performance was dramatically and equivalently enhanced in each incentive condition, whereas neural activity dynamics differed between incentive categories. The monetary reward condition was associated with a tonic activation increase in primarily right-lateralized cognitive control regions including anterior prefrontal cortex (PFC), dorsolateral PFC, and parietal cortex. In the liquid condition, the identical regions instead showed a shift in transient activation from a reactive control pattern (primary probe-based activation) during no-incentive trials to proactive control (primary cue-based activation) during rewarded trials. Additionally, liquid-specific tonic activation increases were found in subcortical regions (amygdala, dorsal striatum, nucleus accumbens), indicating an anatomical double dissociation in the locus of sustained activation. Conclusions/Significance These different activation patterns suggest that primary and secondary rewards may produce similar behavioral changes through distinct neural mechanisms of reinforcement. Further, our results provide new evidence for the flexibility of cognitive control, in terms of the temporal dynamics of activation.

Are people really more patient than other animals? Evidence from human discounting of real liquid rewards.

In previous studies, researchers have found that humans discount delayed rewards orders of magnitude less steeply than do other animals. Humans also discount smaller delayed reward amounts more steeply than larger amounts, whereas animals apparently do not. These differences between humans and animals might reflect differences in the types of rewards studied and/or the fact that animals actually had to wait for their rewards. In the present article, we report the results of three experiments in which people made choices involving liquid rewards delivered and consumed after actual delays, thereby bridging the gap between animal and human studies. Under these circumstances, humans, like animals, discounted the value of rewards delayed by seconds; however, unlike animals, they still showed an effect of reward amount. Human discounting was well described by the same hyperboloid function that has previously been shown to describe animal discounting of delayed food and water rewards, as well as human discounting of real and hypothetical monetary rewards.

Impulsivity and Self-Control during Intertemporal Decision Making Linked to the Neural Dynamics of Reward Value Representation

A characteristic marker of impulsive decision making is the discounting of delayed rewards, demonstrated via choice preferences and choice-related brain activity. However, delay discounting may also arise from how subjective reward value is dynamically represented in the brain when anticipating an upcoming chosen reward. In the current study, brain activity was continuously monitored as human participants freely selected an immediate or delayed primary liquid reward and then waited for the specified delay before consuming it. The ventromedial prefrontal cortex (vmPFC) exhibited a characteristic pattern of activity dynamics during the delay period, as well as modulation during choice, that is consistent with the time-discounted coding of subjective value. The ventral striatum (VS) exhibited a similar activity pattern, but preferentially in impulsive individuals. A contrasting profile of delay-related and choice activation was observed in the anterior PFC (aPFC), but selectively in patient individuals. Functional connectivity analyses indicated that both vmPFC and aPFC exerted modulatory, but opposite, influences on VS activation. These results link behavioral impulsivity and self-control to dynamically evolving neural representations of future reward value, not just during choice, but also during postchoice delay periods.

The neural basis of task switching changes with skill acquisition

Learning novel skills involves reorganization and optimization of cognitive processing involving a broad network of brain regions. Previous work has shown asymmetric costs of switching to a well-trained task vs. a poorly-trained task, but the neural basis of these differential switch costs is unclear. The current study examined the neural signature of task switching in the context of acquisition of new skill. Human participants alternated randomly between a novel visual task (mirror-reversed word reading) and a highly practiced one (plain word reading), allowing the isolation of task switching and skill set maintenance. Two scan sessions were separated by 2 weeks, with behavioral training on the mirror reading task in between the two sessions. Broad cortical regions, including bilateral prefrontal, parietal, and extrastriate cortices, showed decreased activity associated with learning of the mirror reading skill. In contrast, learning to switch to the novel skill was associated with decreased activity in a focal subcortical region in the dorsal striatum. Switching to the highly practiced task was associated with a non-overlapping set of regions, suggesting substantial differences in the neural substrates of switching as a function of task skill. Searchlight multivariate pattern analysis also revealed that learning was associated with decreased pattern information for mirror vs. plain reading tasks in fronto-parietal regions. Inferior frontal junction and posterior parietal cortex showed a joint effect of univariate activation and pattern information. These results suggest distinct learning mechanisms task performance and executive control as a function of learning.

Multiple brain networks contribute to the acquisition of bias in perceptual decision-making

Bias occurs in perceptual decisions when the reward associated with a particular response dominates the sensory evidence in support of a choice. However, it remains unclear how this bias is acquired and once acquired, how it influences perceptual decision processes in the brain. We addressed these questions using model-based neuroimaging in a motion discrimination paradigm where contextual cues suggested which one of two options would receive higher rewards on each trial. We found that participants gradually learned to choose the higher-rewarded option in each context when making a perceptual decision. The amount of bias on each trial was fit well by a reinforcement-learning model that estimated the subjective value of each option within the current context. The brain mechanisms underlying this bias acquisition process were similar to those observed in reward-based decision tasks: prediction errors correlated with the fMRI signals in ventral striatum, dlPFC, and parietal cortex, whereas the amount of acquired bias correlated with activity in ventromedial prefrontal (vmPFC), dorsolateral frontal (dlPFC), and parietal cortices. Moreover, psychophysiological interaction analysis revealed that as bias increased, functional connectivity increased within multiple brain networks (dlPFC-vmPFC-visual, vmPFC-motor, and parietal-anterior-cingulate), suggesting that multiple mechanisms contribute to bias in perceptual decisions through integration of value processing with action, sensory, and control systems. These provide a novel link between the neural mechanisms underlying perceptual and economic decision-making.

Involvement of medial prefrontal cortex in emotion during feedback presentation

It has been suggested that the posterior medial prefrontal cortex (pMPFC) implements cognitive functions involved during negative feedback processing. It has also been suggested that the presentation of the feedback elicits emotional processes. This functional MRI study examined whether pMPFC was associated with the emotional component in feedback processing. Participants were exposed to feedback while performing a version of a motion prediction task. The pMPFC was activated during negative feedback presentation and emotion-related activity was extracted from the pMPFC activation through parametric imaging analysis. It was found that the emotional pMPFC activity was greater in participants who scored higher on depressive mood scales. The results suggest that pMPFC also implements feedback-related emotional functions, which individually vary depending on depressive moods.

Intertemporal Decision-Making Involves Prefrontal Control Mechanisms Associated with Working Memory

Intertemporal decision-making involves simultaneous evaluation of both the magnitude and delay to reward, which may require the integrated representation and comparison of these dimensions within working memory (WM). In the current study, neural activation associated with intertemporal decision-making was directly compared with WM load-related activation. During functional magnetic resonance imaging, participants performed an intermixed series of WM trials and intertemporal decision-making trials both varying in load, with the latter in terms of choice difficulty, via options tailored to each participants subjective value function for delayed rewards. The right anterior prefrontal cortex (aPFC) and dorsolateral prefrontal cortex (dlPFC) showed activity modulation by choice difficulty within WM-related brain regions. In aPFC, these 2 effects (WM, choice difficulty) correlated across individuals. In dlPFC, activation increased with choice difficulty primarily in patient (self-controlled) individuals, and moreover was strongest when the delayed reward was chosen on the most difficult trials. Finally, the choice-difficulty effects in dlPFC and aPFC were correlated across individuals, suggesting a functional relationship between the 2 regions. Together, these results suggest a more precise account of the relationship between WM and intertemporal decision-making that is specifically tied to choice difficulty, and involves the coordinated activation of a lateral PFC circuit supporting successful self-control.