Bolton K. H. Chau

A neural mechanism underlying failure of optimal choice with multiple alternatives

Despite widespread interest in neural mechanisms of decision-making, most investigations focus on decisions between just two options. Here we adapt a biophysically plausible model of decision-making to predict how a key decision variable, the value difference signal—encoding how much better one choice is than another—changes with the value of a third, but unavailable, alternative. The model predicts a surprising failure of optimal decision-making: greater difficulty choosing between two options in the presence of a third very poor, as opposed to very good, alternative. Both investigation of human decision-making and functional magnetic resonance imaging–based measurements of value difference signals in ventromedial prefrontal cortex (vmPFC) bore out this prediction. The vmPFC signal decreased in the presence of low-value third alternatives, and vmPFC effect sizes predicted individual variation in suboptimal decision-making in the presence of multiple alternatives. The effect contrasts with that of divisive normalization in parietal cortex.

Contrasting Roles for Orbitofrontal Cortex and Amygdala in Credit Assignment and Learning in Macaques

Summary Recent studies have challenged the view that orbitofrontal cortex (OFC) and amygdala mediate flexible reward-guided behavior. We trained macaques to perform an object discrimination reversal task during fMRI sessions and identified a lateral OFC (lOFC) region in which activity predicted adaptive win-stay/lose-shift behavior. Amygdala and lOFC activity was more strongly coupled on lose-shift trials. However, lOFC-amygdala coupling was also modulated by the relevance of reward information in a manner consistent with a role in establishing how credit for reward should be assigned. Day-to-day fluctuations in signals and signal coupling were correlated with day-to-day fluctuation in performance. A second experiment confirmed the existence of signals for adaptive stay/shift behavior in lOFC and reflecting irrelevant reward in the amygdala in a probabilistic learning task. Our data demonstrate that OFC and amygdala each make unique contributions to flexible behavior and credit assignment.

Predictive decision making driven by multiple time-linked reward representations in the anterior cingulate cortex

In many natural environments the value of a choice gradually gets better or worse as circumstances change. Discerning such trends makes predicting future choice values possible. We show that humans track such trends by comparing estimates of recent and past reward rates, which they are able to hold simultaneously in the dorsal anterior cingulate cortex (dACC). Comparison of recent and past reward rates with positive and negative decision weights is reflected by opposing dACC signals indexing these quantities. The relative strengths of time-linked reward representations in dACC predict whether subjects persist in their current behaviour or switch to an alternative. Computationally, trend-guided choice can be modelled by using a reinforcement-learning mechanism that computes a longer-term estimate (or expectation) of prediction errors. Using such a model, we find a relative predominance of expected prediction errors in dACC, instantaneous prediction errors in the ventral striatum and choice signals in the ventromedial prefrontal cortex.

Prioritising the relevant information for learning and decision making within orbital and ventromedial prefrontal cortex.

Our environment and internal states are frequently complex, ambiguous and dynamic, meaning we need to have selection mechanisms to ensure we are basing our decisions on currently relevant information. Here, we review evidence that orbitofrontal (OFC) and ventromedial prefrontal cortex (VMPFC) play conserved, critical but distinct roles in this process. While OFC may use specific sensory associations to enhance task-relevant information, particularly in the context of learning, VMPFC plays a role in ensuring irrelevant information does not impinge on the decision in hand.

Contrasting effects of medial and lateral orbitofrontal cortex lesions on credit assignment and decision making in humans

The orbitofrontal cortex is critical for goal-directed behavior. Recent work in macaques has suggested the lateral orbitofrontal cortex (lOFC) is relatively more concerned with assignment of credit for rewards to particular choices during value-guided learning, whereas the medial orbitofrontal cortex (often referred to as ventromedial prefrontal cortex in humans; vmPFC/mOFC) is involved in constraining the decision to the relevant options. We examined whether people with damage restricted to subregions of prefrontal cortex showed the patterns of impairment observed in prior investigations of the effects of lesions to homologous regions in macaques. Groups of patients with either lOFC (predominantly right hemisphere), mOFC/vmPFC, or dorsomedial prefrontal (DMF), and a comparison group of healthy age- and education-matched controls performed a probabilistic 3-choice decision-making task. We report anatomically specific patterns of impairment. We found that credit assignment, as indexed by the normal influence of contingent relationships between choice and reward, is reduced in lOFC patients compared with Controls and mOFC/vmPFC patients. Moreover, the effects of reward contingency on choice were similar for patients with lesions in DMF or mOFC/vmPFC, compared with Controls. By contrast, mOFC/vmPFC-lesioned patients made more stochastic choices than Controls when the decision was framed by valuable distracting alternatives, suggesting that value comparisons were no longer independent of irrelevant options. Once again, there was evidence of regional specialization: patients with lOFC lesions were unimpaired relative to Controls. As in macaques, human lOFC and mOFC/vmPFC are necessary for contingent learning and value-guided decision-making, respectively. SIGNIFICANCE STATEMENT The lateral and medial regions of the orbitofrontal cortex are cytoarchitectonically distinct and have different anatomical connections. Previous investigations in macaques have shown these anatomical differences are accompanied by functional specialization for learning and decision-making. Here, for the first time, we test the predictions made by macaque studies in an experiment with humans with frontal lobe lesions, asking whether behavioral impairments can be linked to lateral or medial orbitofrontal cortex. Using equivalent tasks and computational analyses, our findings broadly replicate the pattern reported after selective lesions in monkeys. Patients with lateral orbitofrontal damage had impaired credit assignment, whereas damage to medial orbitofrontal cortex meant that patients were more likely to be distracted by irrelevant options.

Salience of Somatosensory Stimulus Modulating External-to-Internal Orienting Attention

Shifting between one’s external and internal environments involves orienting attention. Studies on differentiating subprocesses associated with external-to-internal orienting attention are limited. This study aimed to reveal the characteristics of the disengagement, shifting and reengagement subprocesses by using somatosensory external stimuli and internally generated images. Study participants were to perceive nociceptive external stimuli (External Low (EL) or External High (EH)) induced by electrical stimulations (50 ms) followed by mentally rehearsing learned subnociceptive images (Internal Low (IL) and Internal High (IH)). Behavioral responses and EEG signals of the participants were recorded. The three significant components elicited were: fronto-central negativity (FCN; 128–180 ms), fronto-central P2 (200–260 ms), and central P3 (320–380 ms), which reflected the three subprocesses, respectively. Differences in the FCN and P2 amplitudes during the orienting to the subnociceptive images revealed only in the EH but not EL stimulus condition that are new findings. The results indicated that modulations of the disengagement and shifting processes only happened if the external nociceptive stimuli were of high salience and the external-to-internal incongruence was large. The reengaging process reflected from the amplitude of P3 correlated significantly with attenuation of the pain intensity felt from the external nociceptive stimuli. These findings suggested that the subprocesses underlying external-to-internal orienting attention serve different roles. Disengagement subprocess tends to be stimulus dependent, which is bottom-up in nature. Shifting and reengagement tend to be top-down subprocesses, which taps on cognitive control. This subprocess may account for the attenuation effects on perceived pain intensity after orienting attention.

Motor skill experience modulates executive control for task switching

This study aimed to investigate the effect of types of motor skills, including open and closed skills on enhancing proactive and reactive controls for task switching. Thirty-six athletes in open (n=18) or closed (n=18) sports and a control group (n=18) completed the task-switching paradigm and the simple reaction task. The task-switching paradigm drew on the proactive and reactive control of executive functions, whereas the simple reaction task assessed the processing speed. Significant Validity×Group effect revealed that the participants with open skills had a lower switch cost of response time compared to the other two groups when the task cue was 100% valid; whereas the participants regardless of motor skills had a lower switch cost of response time compared to the control group when the task cue was 50% valid. Hierarchical stepwise regression analysis further confirmed these findings. For the simple reaction task, there were no differences found among the three groups. These findings suggest that experience in open skills has benefits of promoting both proactive and reactive controls for task switching, which corresponds to the activity context exposed by the participants. In contrast, experience in closed skills appears to only benefit development of reactive control for task switching. The neural mechanisms for the proactive and reactive controls of executive functions between experts with open and closed skills call for future study.

The macaque anterior cingulate cortex translates counterfactual choice value into actual behavioral change

The neural mechanisms mediating sensory-guided decision making have received considerable attention but animals often pursue behaviors for which there is currently no sensory evidence. Such behaviors are guided by internal representations of choice values that have to be maintained even when these choices are unavailable. We investigated how four macaque monkeys maintained representations of the value of counterfactual choices – choices that could not be taken at the current moment but which could be taken in the future. Using functional magnetic resonance imaging, we found two different patterns of activity co-varying with values of counterfactual choices in a circuit spanning hippocampus, anterior lateral prefrontal cortex, and anterior cingulate cortex (ACC). ACC activity also reflected whether the internal value representations would be translated into actual behavioral change. To establish the causal importance of ACC for this translation process, we used a novel technique, Transcranial Focused Ultrasound Stimulation, to reversibly disrupt ACC activity.

Aging Effect on Audiovisual Integrative Processing in Spatial Discrimination Task

Multisensory integration is an essential process that people employ daily, from conversing in social gatherings to navigating the nearby environment. The aim of this study was to investigate the impact of aging on modulating multisensory integrative processes using event-related potential (ERP), and the validity of the study was improved by including “noise” in the contrast conditions. Older and younger participants were involved in perceiving visual and/or auditory stimuli that contained spatial information. The participants responded by indicating the spatial direction (far vs. near and left vs. right) conveyed in the stimuli using different wrist movements. electroencephalograms (EEGs) were captured in each task trial, along with the accuracy and reaction time of the participants’ motor responses. Older participants showed a greater extent of behavioral improvements in the multisensory (as opposed to unisensory) condition compared to their younger counterparts. Older participants were found to have fronto-centrally distributed super-additive P2, which was not the case for the younger participants. The P2 amplitude difference between the multisensory condition and the sum of the unisensory conditions was found to correlate significantly with performance on spatial discrimination. The results indicated that the age-related effect modulated the integrative process in the perceptual and feedback stages, particularly the evaluation of auditory stimuli. Audiovisual (AV) integration may also serve a functional role during spatial-discrimination processes to compensate for the compromised attention function caused by aging.

Potential application of cross-modal stimulation for neurorehabilitation : the relatedness of performance on tasks measuring cognitive processes subserved by similar prefrontal substrates

OBJECTIVE Rehabilitating people with prefrontal functional impairment has always been challenging. This study examined whether there are functional relationships between prefrontal processes subserved by similar neural regions. The aim was to shed light on the therapeutic potential of training one function to effect changes in another function, a phenomenon called cross-modal stimulation in neurorehabilitation. The study examined risky decision-making by people of high or low odour-identification ability because both processes are subserved by the orbitofrontal regions. METHOD This question was examined in a sample of women (n = 44) with high or low odour-identification ability, classified according to their performance on the Odour Identification Test. Their risky decision-making was measured by the Risky Gains Task. RESULTS The women with better odour-identification ability made more risky decisions. However, there was no such difference on another cognitive task (Choice RT and Suppress Test), the processing of which involves frontal substrates other than the orbitofrontal region. CONCLUSION These findings provide preliminary insight into the phenomenon that performance on tests of prefrontal functions could relate to each other if the functions share similar prefrontal substrates.