Anterior Cingulate Cortex Signals Research Articles

Attention for Learning Signals in Anterior Cingulate Cortex

Learning theory suggests that animals attend to pertinent environmental cues when reward contingencies unexpectedly change so that learning can occur. We have previously shown that activity in basolateral nucleus of amygdala (ABL) responds to unexpected changes in reward value, consistent with unsigned prediction error signals theorized by Pearce and Hall. However, changes in activity were present only at the time of unexpected reward delivery, not during the time when the animal needed to attend to conditioned stimuli that would come to predict the reward. This suggested that a different brain area must be signaling the need for attention necessary for learning. One likely candidate to fulfill this role is the anterior cingulate cortex (ACC). To test this hypothesis, we recorded from single neurons in ACC as rats performed the same behavioral task that we have used to dissociate signed from unsigned prediction errors in dopamine and ABL neurons. In this task, rats chose between two fluid wells that produced varying magnitudes of and delays to reward. Consistent with previous work, we found that ACC detected errors of commission and reward prediction errors. We also found that activity during cue sampling encoded reward size, but not expected delay to reward. Finally, activity in ACC was elevated during trials in which attention was increased following unexpected upshifts and downshifts in value. We conclude that ACC not only signals errors in reward prediction, as previously reported, but also signals the need for enhanced neural resources during learning on trials subsequent to those errors.

The anterior cingulate cortex: Monitoring the outcomes of others' decisions

The ability to attribute mental states to others and understand the basis of their decisions is essential for human social interaction. A controversial theory states that this is achieved by simulating another's information processing in one's own neural circuits. The anterior cingulate cortex (ACC) is known to play an important role in the registration of discrepancies between the predicted and actual outcomes of decisions (prediction errors).When positive and negative feedback fails altogether, the failure may also signal errors in the prediction that the outcome of that decision would be informative and guide future decisions. Does the ACC signal that an outcome is unexpectedly uninformative? When an outcome directed to others is uninformative, do we understand their mental states by simulating them in the circuits of the ACC in our own brain? The aim of our study was to test for these two possibilities in the human brain with event-related fMRI. We tested whether the ACC processes errors in the prediction of informative feedback and whether the ACC is also activated when scanned subjects process the same outcomes of another's decisions. We show that each is processed by a separate subregion of the ACC.

Separate encoding of model-based and model-free valuations in the human brain

Behavioral studies have long shown that humans solve problems in two ways, one intuitive and fast (System 1, model-free), and the other reflective and slow (System 2, model-based). The neurobiological basis of dual process problem solving remains unknown due to challenges of separating activation in concurrent systems. We present a novel neuroeconomic task that predicts distinct subjective valuation and updating signals corresponding to these two systems. We found two concurrent value signals in human prefrontal cortex: a System 1 model-free reinforcement signal and a System 2 model-based Bayesian signal. We also found a System 1 updating signal in striatal areas and a System 2 updating signal in lateral prefrontal cortex. Further, signals in prefrontal cortex preceded choices that are optimal according to either updating principle, while signals in anterior cingulate cortex and globus pallidus preceded deviations from optimal choice for reinforcement learning. These deviations tended to occur when uncertainty regarding optimal values was highest, suggesting that disagreement between dual systems is mediated by uncertainty rather than conflict, confirming recent theoretical proposals.

Surprise Signals in Anterior Cingulate Cortex: Neuronal Encoding of Unsigned Reward Prediction Errors Driving Adjustment in Behavior

In attentional models of learning, associations between actions and subsequent rewards are stronger when outcomes are surprising, regardless of their valence. Despite the behavioral evidence that surprising outcomes drive learning, neural correlates of unsigned reward prediction errors remain elusive. Here we show that in a probabilistic choice task, trial-to-trial variations in preference track outcome surprisingness. Concordant with this behavioral pattern, responses of neurons in macaque (Macaca mulatta) dorsal anterior cingulate cortex (dACC) to both large and small rewards were enhanced when the outcome was surprising. Moreover, when, on some trials, probabilities were hidden, neuronal responses to rewards were reduced, consistent with the idea that the absence of clear expectations diminishes surprise. These patterns are inconsistent with the idea that dACC neurons track signed errors in reward prediction, as dopamine neurons do. Our results also indicate that dACC neurons do not signal conflict. In the context of other studies of dACC function, these results suggest a link between reward-related modulations in dACC activity and attention and motor control processes involved in behavioral adjustment. More speculatively, these data point to a harmonious integration between reward and learning accounts of ACC function on one hand, and attention and cognitive control accounts on the other.

To Bet or Not to Bet? The Error Negativity or Error-related Negativity Associated with Risk-taking Choices

The functional significance of error-related negativity (Ne/ERN), which occurs at approximately the same time as erroneous responses, has been investigated extensively using reaction time (RT) tasks. The error detection theory assumes that the Ne/ERN reflects the mismatch detected by comparing representations of the intended and the actually performed actions. The conflict monitoring theory asserts that the Ne/ERN reflects the detection of response conflict between intended and actually performed actions during response selection. In this study, we employed a gambling task in which participants were required to choose whether they would take part in betting in each trial and they were presented with gain or loss feedback in both the "to bet" and the "not to bet" trials. The response-locked ERP magnitudes were more negative for "to bet" than for "not to bet" choices for both large and small stakes and were more negative for choices involving large rather than small stakes. Dipole source analysis localized the ERP responses to the anterior cingulate cortex (ACC). These findings suggest that the ACC signals the riskiness of choices and may function as an early warning system that alerts the brain to prepare for the potential negative consequence associated with a risky action.

Anterior cingulate cortex signals the requirement to break inertia when switching tasks: A study of the bivalency effect

When switching tasks, if stimuli are presented that cue two of the tasks in the task set (i.e., bivalent stimuli), performance slowing is observed on all tasks, including those not cued by the bivalent stimulus. This slowing has been coined the bivalency effect, and may reflect adaptive tuning of the response style under conditions that appear to require adjustments in control over the course of action. Recent work on the function of the dorsal anterior cingulate (dACC) cortex has suggested that this neural region may be recruited under such conditions. In the current task switching study, we used tightly matched experimental and control conditions to isolate the bivalency effect. As predicted, dACC activation was associated with the bivalency effect, supporting an account stating that the role of the dACC is to signal a break in task inertia in order to adaptively tune the response style due to conditions that may require adjustments in control over the course of action. This result may extend the conflict monitoring account of dACC activation to situations where conflict occurred on past trials (i.e., conflict is not elicited by the current stimulus), and/or may support a more generalized account of dACC function involving monitoring internal states for conditions that may require adjustments in control over the course of action.

Executive control of gaze by the frontal lobes

Executive control requires controlling the initiation of movements, judging the consequences of actions, and adjusting performance accordingly. We have investigated the role of different areas in the frontal lobe in executive control expressed by macaque monkeys performing a saccade stop signal task. Certain neurons in the frontal eye field respond to visual stimuli, and others control the production of saccadic eye movements. Neurons in the supplementary eye field do not control directly the initiation of saccades but, instead, signal the production of errors, the anticipation and delivery of reinforcement, and the presence of response conflict. Neurons in the anterior cingulate cortex signal the production of errors and the anticipation and delivery of reinforcement, but not the presence of response conflict. Intracranial local field potentials in the anterior cingulate cortex of monkeys indicate that these medial frontal signals can contribute to event-related potentials related to performance monitoring. Electrical stimulation of the supplementary eye field improves performance in the task by elevating saccade latency. An interactive race model shows how interacting units produce behavior that can be described as the outcome of a race between independent processes and how conflict between gaze-holding and gaze-shifting neurons can be used to adjust performance.

Learning the value of information in an uncertain world

Our decisions are guided by outcomes that are associated with decisions made in the past. However, the amount of influence each past outcome has on our next decision remains unclear. To ensure optimal decision-making, the weight given to decision outcomes should reflect their salience in predicting future outcomes, and this salience should be modulated by the volatility of the reward environment. We show that human subjects assess volatility in an optimal manner and adjust decision-making accordingly. This optimal estimate of volatility is reflected in the fMRI signal in the anterior cingulate cortex (ACC) when each trial outcome is observed. When a new piece of information is witnessed, activity levels reflect its salience for predicting future outcomes. Furthermore, variations in this ACC signal across the population predict variations in subject learning rates. Our results provide a formal account of how we weigh our different experiences in guiding our future actions.

Modafinil modulates anterior cingulate function in chronic schizophrenia

Schizophrenia is associated with widespread cognitive deficits that have an impact on social function. Modafinil promotes wakefulness and is reported to enhance cognition. To study the acute effects of modafinil administration upon brain activity and cognitive performance in people with chronic schizophrenia. In a randomised double-blind placebo-controlled crossover design, 19 patients received either modafinil (100 mg) or placebo prior to undertaking a working memory task with functional magnetic resonance imaging. Seventeen patients completed the study and another underwent acute relapse 4 days post-drug. Modafinil administration was associated with significantly greater activation in the anterior cingulate cortex during the working memory task. The anterior cingulate cortex signal correlated with cognitive performance, although only a subset of patients exhibited 'enhancement'. Modafinil modulates anterior cingulate cortex function in chronic schizophrenia but its beneficial cognitive effects may be restricted to a subset of patients requiring further characterisation.

Debate: euthanasia--a physician's viewpoint.

Discussion about euthanasia is often confused because of a failure to distinguish between deliberate death acceleration and letting nature take its course. There is a need to reiterate the traditional principles upon which the care of the dying should be based, including the need for the doctor to practise medicine in the knowledge that eventually all his patients will die. It follows that a doctor does not have a duty to preserve life at all costs. The care of the patient with far-advanced cancer has improved considerably in many areas as a result of the establishment of hospices and domiciliary support teams. Treating the patient as a person is the key to a successful doctor-patient relationship. An analytical approach is necessary to control pain and other symptoms. Care of the relatives is also fundamental. Voluntary euthanasia and 'assisted suicide' represent an extreme solution to a situation which demands a far more comprehensive and compassionate approach. The need is not for a change in the law but for a change of emphasis in medical education.