Kenji Matsumoto

Medial prefrontal cell activity signaling prediction errors of action values

To adapt behavior to a changing environment, one must monitor outcomes of executed actions and adjust subsequent actions accordingly. Involvement of the medial frontal cortex in performance monitoring has been suggested, but little is known about neural processes that link performance monitoring to performance adjustment. Here, we recorded from neurons in the medial prefrontal cortex of monkeys learning arbitrary action-outcome contingencies. Some cells preferentially responded to positive visual feedback stimuli and others to negative feedback stimuli. The magnitude of responses to positive feedback stimuli decreased over the course of behavioral adaptation, in correlation with decreases in the amount of prediction error of action values. Therefore, these responses in medial prefrontal cells may signal the direction and amount of error in prediction of values of executed actions to specify the adjustment in subsequent action selections.

Neural basis of the undermining effect of monetary reward on intrinsic motivation

Contrary to the widespread belief that people are positively motivated by reward incentives, some studies have shown that performance-based extrinsic reward can actually undermine a persons intrinsic motivation to engage in a task. This “undermining effect” has timely practical implications, given the burgeoning of performance-based incentive systems in contemporary society. It also presents a theoretical challenge for economic and reinforcement learning theories, which tend to assume that monetary incentives monotonically increase motivation. Despite the practical and theoretical importance of this provocative phenomenon, however, little is known about its neural basis. Herein we induced the behavioral undermining effect using a newly developed task, and we tracked its neural correlates using functional MRI. Our results show that performance-based monetary reward indeed undermines intrinsic motivation, as assessed by the number of voluntary engagements in the task. We found that activity in the anterior striatum and the prefrontal areas decreased along with this behavioral undermining effect. These findings suggest that the corticobasal ganglia valuation system underlies the undermining effect through the integration of extrinsic reward value and intrinsic task value.

Prefrontal cell activities related to monkeys' success and failure in adapting to rule changes in a Wisconsin Card Sorting Test analog.

The cognitive flexibility to select appropriate rules in a changing environment is essential for survival and is assumed to depend on the integrity of prefrontal cortex (PFC). To explore the contribution of the dorsolateral PFC to flexible rule-based behavior, we recorded the activity of cells in this region of monkeys performing a Wisconsin Card Sorting Test (WCST) analog. The monkey had to match a sample to one of three test items by either color or shape. Liquid reward and a discrete visual signal (error signal) were given as feedback to correct and incorrect target selections, respectively. The relevant rule and its frequent changes were not cued, and the monkeys could find it only by interpreting the feedback. In one-third of cells, cellular activity was modulated by the relevant rule, both throughout the trial and between trials. The magnitude of the modulation correlated with the number of errors that the monkeys committed after each rule change in the course of reestablishing high performance. Activity of other cells differed between correct and error trials independently from the rule-related modulation. This difference appeared during actual responses and before the monkeys faced the problems. Many PFC cells responded to the error-signal presentation, and, in some of them, the magnitude of response depended on the relevant rule. These results suggest that the dorsolateral PFC contributes to WCST performance by maintaining the relevant rule across trials, assessing behavioral outcomes, and monitoring the processes that could lead to success and failure in individual trials.

Neural correlates of cognitive dissonance and choice-induced preference change

According to many modern economic theories, actions simply reflect an individuals preferences, whereas a psychological phenomenon called “cognitive dissonance” claims that actions can also create preference. Cognitive dissonance theory states that after making a difficult choice between two equally preferred items, the act of rejecting a favorite item induces an uncomfortable feeling (cognitive dissonance), which in turn motivates individuals to change their preferences to match their prior decision (i.e., reducing preference for rejected items). Recently, however, Chen and Risen [Chen K, Risen J (2010) J Pers Soc Psychol 99:573–594] pointed out a serious methodological problem, which casts a doubt on the very existence of this choice-induced preference change as studied over the past 50 y. Here, using a proper control condition and two measures of preferences (self-report and brain activity), we found that the mere act of making a choice can change self-report preference as well as its neural representation (i.e., striatum activity), thus providing strong evidence for choice-induced preference change. Furthermore, our data indicate that the anterior cingulate cortex and dorsolateral prefrontal cortex tracked the degree of cognitive dissonance on a trial-by-trial basis. Our findings provide important insights into the neural basis of how actions can alter an individuals preferences.

The role of the medial prefrontal cortex in achieving goals

Achieving goals in changing environments requires the course of action to be selected on the basis of goal expectation and memory of action-outcome contingency. It is often also essential to evaluate action on the basis of immediate outcomes and the discrimination of early action steps from the final step towards the goal. Recently, in single-cell recordings in monkeys, the neuronal activity that appears to underlie these processes has been noted in the medial part of the prefrontal cortex. Medial prefrontal cells were also active when the subjects extracted the rules of a task in a novel environment. The processes described above might play important roles in rule learning.

How Self-Determined Choice Facilitates Performance: A Key Role of the Ventromedial Prefrontal Cortex

Recent studies have documented that self-determined choice does indeed enhance performance. However, the precise neural mechanisms underlying this effect are not well understood. We examined the neural correlates of the facilitative effects of self-determined choice using functional magnetic resonance imaging (fMRI). Participants played a game-like task involving a stopwatch with either a stopwatch they selected (self-determined-choice condition) or one they were assigned without choice (forced-choice condition). Our results showed that self-determined choice enhanced performance on the stopwatch task, despite the fact that the choices were clearly irrelevant to task difficulty. Neuroimaging results showed that failure feedback, compared with success feedback, elicited a drop in the vmPFC activation in the forced-choice condition, but not in the self-determined-choice condition, indicating that negative reward value associated with the failure feedback vanished in the self-determined-choice condition. Moreover, the vmPFC resilience to failure in the self-determined-choice condition was significantly correlated with the increased performance. Striatal responses to failure and success feedback were not modulated by the choice condition, indicating the dissociation between the vmPFC and striatal activation pattern. These findings suggest that the vmPFC plays a unique and critical role in the facilitative effects of self-determined choice on performance.

Neuronal Responses to Object Images in the Macaque Inferotemporal Cortex at Different Stimulus Discrimination Levels

We can discriminate visual objects at multiple levels, from coarse categorization to individual identification. It is not known how the brain adapts to the varying levels of discrimination required in different behavioral contexts. In the present study, we investigated whether the stimulus selectivity of neuronal responses in the monkey inferotemporal cortex, which is the final unimodal stage in the ventral visual pathway, changes with the varying levels of discrimination required for different task conditions. Responses of each inferotemporal cell to the same set of nine object images were examined in two different task conditions. The task alternated between coarse and fine discriminations in the first experiment, and the rule alternated between categorization and individual object identification in the second experiment. Despite these changes in the task requirements and the resulting differences in the monkeys behavior, we found that the responses of inferotemporal cells were largely unchanged in both experiments. Our results suggest that representation of object images in the inferotemporal cortex is stable and rather insensitive to these kinds of shifts in behavioral context. Neuronal adaptations to behavioral context may occur downstream of the inferotemporal cortex.

Social Equality in the Number of Choice Options Is Represented in the Ventromedial Prefrontal Cortex

A distinct aspect of the sense of fairness in humans is that we care not only about equality in material rewards but also about equality in nonmaterial values. One such value is the opportunity to choose freely among many options, often regarded as a fundamental right to economic freedom. In modern developed societies, equal opportunities in work, living, and lifestyle are enforced by antidiscrimination laws. Despite the widespread endorsement of equal opportunity, no studies have explored how people assign value to it. We used functional magnetic resonance imaging to identify the neural substrates for subjective valuation of equality in choice opportunity. Participants performed a two-person choice task in which the number of choices available was varied across trials independently of choice outcomes. By using this procedure, we manipulated the degree of equality in choice opportunity between players and dissociated it from the value of reward outcomes and their equality. We found that activation in the ventromedial prefrontal cortex (vmPFC) tracked the degree to which the number of options between the two players was equal. In contrast, activation in the ventral striatum tracked the number of options available to participants themselves but not the equality between players. Our results demonstrate that the vmPFC, a key brain region previously implicated in the processing of social values, is also involved in valuation of equality in choice opportunity between individuals. These findings may provide valuable insight into the human ability to value equal opportunity, a characteristic long emphasized in politics, economics, and philosophy.

Effects of novelty on activity of lateral and medial prefrontal neurons

Detection of novel events is crucial for adapting to changing environments. The prefrontal cortex has been thought to be one of the areas involved in orienting attention to novel events. Here, we examined the effects of two components of novelty: context novelty, which purely happens when a familiar event occurs in an unpredicted situation or time and feature novelty, which happens by itself when an unfamiliar stimulus appears against the expectation of familiar ones. We trained monkeys on a task that included both novelty components and recorded the activity of neurons in the lateral and medial divisions of the prefrontal cortex. The responses of a substantial number of cells in both the lateral and medial divisions were enhanced when a familiar visual stimulus was presented in an unpredicted context. By contrast, enhancement of responses by the unfamiliarity of visual stimuli was observed mainly in cells in the lateral prefrontal cortex. These results suggest that the lateral and medial divisions of the prefrontal cortex are differentially involved in the control of attention triggered by novel sensory events.

Human neural responses involved in spatial pooling of locally ambiguous motion signals

Early visual motion signals are local and one-dimensional (1-D). For specification of global two-dimensional (2-D) motion vectors, the visual system should appropriately integrate these signals across orientation and space. Previous neurophysiological studies have suggested that this integration process consists of two computational steps (estimation of local 2-D motion vectors, followed by their spatial pooling), both being identified in the area MT. Psychophysical findings, however, suggest that under certain stimulus conditions, the human visual system can also compute mathematically correct global motion vectors from direct pooling of spatially distributed 1-D motion signals. To study the neural mechanisms responsible for this novel 1-D motion pooling, we conducted human magnetoencephalography (MEG) and functional MRI experiments using a global motion stimulus comprising multiple moving Gabors (global-Gabor motion). In the first experiment, we measured MEG and blood oxygen level-dependent responses while changing motion coherence of global-Gabor motion. In the second experiment, we investigated cortical responses correlated with direction-selective adaptation to the global 2-D motion, not to local 1-D motions. We found that human MT complex (hMT+) responses show both coherence dependency and direction selectivity to global motion based on 1-D pooling. The results provide the first evidence that hMT+ is the locus of 1-D motion pooling, as well as that of conventional 2-D motion pooling.