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Complementary encoding of priors in monkey frontoparietal network supports a dual process of decision-making.

ABSTRACT: Prior expectations of movement instructions can promote preliminary action planning and influence choices. We investigated how action priors affect action-goal encoding in premotor and parietal cortices and if they bias subsequent free choice. Monkeys planned reaches according to visual cues that indicated relative probabilities of two possible goals. On instructed trials, the reach goal was determined by a secondary cue respecting these probabilities. On rarely interspersed free-choice trials without instruction, both goals offered equal reward. Action priors induced graded free-choice biases and graded frontoparietal motor-goal activity, complementarily in two subclasses of neurons. Down-regulating neurons co-encoded both possible goals and decreased opposite-to-preferred responses with decreasing prior, possibly supporting a process of choice by elimination. Up-regulating neurons showed increased preferred-direction responses with increasing prior, likely supporting a process of computing net likelihood. Action-selection signals emerged earliest in down-regulating neurons of premotor cortex, arguing for an initiation of selection in the frontal lobe.

SUBMITTER: Suriya-Arunroj L

PROVIDER: S-EPMC6794075 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Complementary encoding of priors in monkey frontoparietal network supports a dual process of decision-making.

Suriya-Arunroj Lalitta L Gail Alexander A

eLife 20191015

Prior expectations of movement instructions can promote preliminary action planning and influence choices. We investigated how action priors affect action-goal encoding in premotor and parietal cortices and if they bias subsequent free choice. Monkeys planned reaches according to visual cues that indicated relative probabilities of two possible goals. On <i>instructed</i> trials, the reach goal was determined by a secondary cue respecting these probabilities. On rarely interspersed <i>free-choic ...[more]

PMID: 31612855

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Project description:Previous single-site neurostimulation experiments have unsuccessfully attempted to shift decision-making away from habitual control, a fast, inflexible cognitive strategy, towards goal-directed control, a flexible, though computationally expensive strategy. We employed a dual-target neurostimulation approach in 30 healthy participants, using cortico-cortical paired associative stimulation (ccPAS) to target two key nodes: lateral prefrontal cortex (LPFC) and intraparietal sulcus (IPS), to test whether decision-making can be artificially shifted from habitual toward goal-directed control. Participants received three active stimulations, delivered at least six days apart (each involving 100 paired pulses over the IPS and LPFC, varying the interstimulus interval): two interventional, time-relevant ccPAS (10 msec interval) and one control, non-time-relevant ccPAS (100 msec interval). Following stimulation, participants completed a sequential learning task, measuring goal-directed/habitual control, and a working memory task. IPS→LPFC ccPAS (stimulating IPS, then LPFC with a 10 msec interval) shifted decision-making from habitual toward goal-directed control, compared to control ccPAS. There was no effect of LPFC→IPS ccPAS, nor an effect of any PAS condition on working memory. Previous studies have shown ccPAS effects outside the motor domain targeting prefrontal regions on response inhibition, attentional bias, and alpha asymmetry. The present study measures the behavioural effects of parietal-prefrontal PAS, focusing on a highly complex decision-making task and working memory. If confirmed in larger studies, this would be the first instance of neurostimulation successfully shifting decision-making from habitual to goal-directed control, putatively via inducing long-term potentiation between the IPS and LPFC. However, we found no effect in the other direction (LPFC→IPS ccPAS), and no effect on working memory overall. PAS is a relatively new neuromodulatory technique in the cognitive arsenal, and this study could help guide future approaches in healthy and disordered decision-making.

Project description:BackgroundDual processing theory of human cognition postulates that reasoning and decision-making can be described as a function of both an intuitive, experiential, affective system (system I) and/or an analytical, deliberative (system II) processing system. To date no formal descriptive model of medical decision-making based on dual processing theory has been developed. Here we postulate such a model and apply it to a common clinical situation: whether treatment should be administered to the patient who may or may not have a disease.MethodsWe developed a mathematical model in which we linked a recently proposed descriptive psychological model of cognition with the threshold model of medical decision-making and show how this approach can be used to better understand decision-making at the bedside and explain the widespread variation in treatments observed in clinical practice.ResultsWe show that physician's beliefs about whether to treat at higher (lower) probability levels compared to the prescriptive therapeutic thresholds obtained via system II processing is moderated by system I and the ratio of benefit and harms as evaluated by both system I and II. Under some conditions, the system I decision maker's threshold may dramatically drop below the expected utility threshold derived by system II. This can explain the overtreatment often seen in the contemporary practice. The opposite can also occur as in the situations where empirical evidence is considered unreliable, or when cognitive processes of decision-makers are biased through recent experience: the threshold will increase relative to the normative threshold value derived via system II using expected utility threshold. This inclination for the higher diagnostic certainty may, in turn, explain undertreatment that is also documented in the current medical practice.ConclusionsWe have developed the first dual processing model of medical decision-making that has potential to enrich the current medical decision-making field, which is still to the large extent dominated by expected utility theory. The model also provides a platform for reconciling two groups of competing dual processing theories (parallel competitive with default-interventionalist theories).

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Complementary encoding of priors in monkey frontoparietal network supports a dual process of decision-making.

Publications

Complementary encoding of priors in monkey frontoparietal network supports a dual process of decision-making.

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