Joshua W. Brown

Medial prefrontal cortex as an action-outcome predictor

The medial prefrontal cortex (mPFC) and especially anterior cingulate cortex is central to higher cognitive function and many clinical disorders, yet its basic function remains in dispute. Various competing theories of mPFC have treated effects of errors, conflict, error likelihood, volatility and reward, using findings from neuroimaging and neurophysiology in humans and monkeys. No single theory has been able to reconcile and account for the variety of findings. Here we show that a simple model based on standard learning rules can simulate and unify an unprecedented range of known effects in mPFC. The model reinterprets many known effects and suggests a new view of mPFC, as a region concerned with learning and predicting the likely outcomes of actions, whether good or bad. Cognitive control at the neural level is then seen as a result of evaluating the probable and actual outcomes of ones actions.

Computational perspectives on dopamine function in prefrontal cortex.

Dopamine and the prefrontal cortex are critical for thought and behaviour. Recently, computational models have tried to elucidate the specific and intricate roles of dopamine in the prefrontal cortex, at the neurophysiological, system and behavioral levels, with varying degrees of success.

Monitoring and Control of Action by the Frontal Lobes

Success requires deciding among alternatives, controlling the initiation of movements, and judging the consequences of actions. When alternatives are difficult to distinguish, habitual responses must be overcome, or consequences are uncertain, deliberation is necessary and a supervisory system exerts control over the processes that produce sensory-guided movements. We have investigated these processes by recording neural activity in the frontal lobe of macaque monkeys performing a countermanding task. Distinct neurons in the frontal eye field respond to visual stimuli or control the production of the movements. In the supplementary eye field and anterior cingulate cortex, neurons appear not to control directly movement initiation but instead signal the production of errors, the anticipation and delivery of reinforcement, and the presence of processing conflict. These signals form the core of current models of supervisory control of sensorimotor processes.

How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades

How does the brain learn to balance between reactive and planned behaviors? The basal ganglia (BG) and frontal cortex together allow animals to learn planned behaviors that acquire rewards when prepotent reactive behaviors are insufficient. This paper proposes a new model, called TELOS, to explain how laminar circuitry of the frontal cortex, exemplified by the frontal eye fields, interacts with the BG, thalamus, superior colliculus, and inferotemporal and parietal cortices to learn and perform reactive and planned eye movements. The model is formulated as fourteen computational hypotheses. These specify how strategy priming and action planning (in cortical layers III, Va and VI) are dissociated from movement execution (in layer Vb), how the BG help to choose among and gate competing plans, and how a visual stimulus may serve either as a movement target or as a discriminative cue to move elsewhere. The direct, indirect and hyperdirect pathways through the BG are shown to enable complex gating functions, including deferred execution of selected plans, and switching among alternative sensory-motor mappings. Notably, the model can learn and gate the use of a What-to-Where transformation that enables spatially invariant object representations to selectively excite spatially coded movement plans. Model simulations show how dopaminergic reward and non-reward signals guide monkeys to learn and perform saccadic eye movements in the fixation, single saccade, overlap, gap, and delay (memory-guided) saccade tasks. Model cell activation dynamics quantitatively simulate seventeen established types of dynamics exhibited by corresponding real cells during performance of these tasks.

A computational model of fractionated conflict-control mechanisms in task-switching

A feature of human cognition is the ability to monitor and adjust ones own behavior under changing circumstances. A dynamic balance between controlled and rapid responding is needed to adapt to a fluctuating environment. We suggest that cognitive control may include, among other things, two distinct processes. Incongruent stimuli may drive top-down facilitation of task-relevant responses to bias performance toward exploitation vs. exploration. Task or response switches may generally slow responses to bias toward accuracy vs. speed and exploration vs. exploitation. Behavioral results from a task switching study demonstrate these two distinct processes as revealed by higher-order sequential effects. A computational model implements the two conflict-control mechanisms, which allow it to capture many complex and novel sequential effects. Lesion studies with the model demonstrate that the model is unable to capture these effects without the conflict-control loops and show how each monitoring component modulates cognitive control. The results suggest numerous testable predictions regarding the neural substrates of cognitive control.

Influence of history on saccade countermanding performance in humans and macaque monkeys

The stop-signal or countermanding task probes the ability to control action by requiring subjects to withhold a planned movement in response to an infrequent stop signal which they do with variable success depending on the delay of the stop signal. We investigated whether performance of humans and macaque monkeys in a saccade countermanding task was influenced by stimulus and performance history. In spite of idiosyncrasies across subjects several trends were evident in both humans and monkeys. Response time decreased after successive trials with no stop signal. Response time increased after successive trials with a stop signal. However, post-error slowing was not observed. Increased response time was observed mainly or only after cancelled (signal inhibit) trials and not after noncancelled (signal respond) trials. These global trends were based on rapid adjustments of response time in response to momentary fluctuations in the fraction of stop signal trials. The effects of trial sequence on the probability of responding were weaker and more idiosyncratic across subjects when stop signal fraction was fixed. However, both response time and probability of responding were influenced strongly by variations in the fraction of stop signal trials. These results indicate that the race model of countermanding performance requires extension to account for these sequential dependencies and provide a basis for physiological studies of executive control of countermanding saccade performance.

Risk prediction and aversion by anterior cingulate cortex

The recently proposed error-likelihood hypothesis suggests that anterior cingulate cortex (ACC) and surrounding areas will become active in proportion to the perceived likelihood of an error. The hypothesis was originally derived from a computational model prediction. The same computational model now makes a further prediction that ACC will be sensitive not only to predicted error likelihood, but also to the predicted magnitude of the consequences, should an error occur. The product of error likelihood and predicted error consequence magnitude collectively defines the general “expected risk” of a given behavior in a manner analogous but orthogonal to subjective expected utility theory. New fMRI results from an incentive change signal task now replicate the errorlikelihood effect, validate the further predictions of the computational model, and suggest why some segments of the population may fail to show an error-likelihood effect. In particular, error-likelihood effects and expected risk effects in general indicate greater sensitivity to earlier predictors of errors and are seen in risk-averse but not risktolerant individuals. Taken together, the results are consistent with an expected risk model of ACC and suggest that ACC may generally contribute to cognitive control by recruiting brain activity to avoid risk.

Error Effects in Anterior Cingulate Cortex Reverse when Error Likelihood Is High

Strong error-related activity in medial prefrontal cortex (mPFC) has been shown repeatedly with neuroimaging and event-related potential studies for the last several decades. Multiple theories have been proposed to account for error effects, including comparator models and conflict detection models, but the neural mechanisms that generate error signals remain in dispute. Typical studies use relatively low error rates, confounding the expectedness and the desirability of an error. Here we show with a gambling task and functional magnetic resonance imaging that when losses are more frequent than wins, the mPFC error effect disappears, and moreover, exhibits the opposite pattern by responding more strongly to unexpected wins than losses. These findings provide perspective on recent ERP studies and suggest that mPFC error effects result from a comparison between actual and expected outcomes.

Role of supplementary eye field in saccade initiation: executive, not direct, control.

The goal of this study was to determine whether the activity of neurons in the supplementary eye field (SEF) is sufficient to control saccade initiation in macaque monkeys performing a saccade countermanding (stop signal) task. As previously observed, many neurons in the SEF increase the discharge rate before saccade initiation. However, when saccades are canceled in response to a stop signal, effectively no neurons with presaccadic activity display discharge rate modulation early enough to contribute to saccade cancellation. Moreover, SEF neurons do not exhibit a specific threshold discharge rate that could trigger saccade initiation. Yet, we observed more subtle relations between SEF activation and saccade production. The activity of numerous SEF neurons was correlated with response time and varied with sequential adjustments in response latency. Trials in which monkeys canceled or produced a saccade in a stop signal trial were distinguished by a modest difference in discharge rate of these SEF neurons before stop signal or target presentation. These findings indicate that neurons in the SEF, in contrast to counterparts in the frontal eye field and superior colliculus, do not contribute directly and immediately to the initiation of visually guided saccades. However the SEF may proactively regulate saccade production by biasing the balance between gaze-holding and gaze-shifting based on prior performance and anticipated task requirements.

Functional heterogeneity of conflict, error, task-switching, and unexpectedness effects within medial prefrontal cortex

The last decade has seen considerable discussion regarding a theoretical account of medial prefrontal cortex (mPFC) function with particular focus on the anterior cingulate cortex. The proposed theories have included conflict detection, error likelihood prediction, volatility monitoring, and several distinct theories of error detection. Arguments for and against particular theories often treat mPFC as functionally homogeneous, or at least nearly so, despite some evidence for distinct functional subregions. Here we used functional magnetic resonance imaging (fMRI) to simultaneously contrast multiple effects of error, conflict, and task-switching that have been individually construed in support of various theories. We found overlapping yet functionally distinct subregions of mPFC, with activations related to dominant error, conflict, and task-switching effects successively found along a rostral-ventral to caudal-dorsal gradient within medial prefrontal cortex. Activations in the rostral cingulate zone (RCZ) were strongly correlated with the unexpectedness of outcomes suggesting a role in outcome prediction and preparing control systems to deal with anticipated outcomes. The results as a whole support a resolution of some ongoing debates in that distinct theories may each pertain to corresponding distinct yet overlapping subregions of mPFC.