scholarly journals Autocorrelation structure at rest predicts value correlates of single neurons during reward-guided choice

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Sean E Cavanagh ◽  
Joni D Wallis ◽  
Steven W Kennerley ◽  
Laurence T Hunt

Correlates of value are routinely observed in the prefrontal cortex (PFC) during reward-guided decision making. In previous work (Hunt et al., 2015), we argued that PFC correlates of chosen value are a consequence of varying rates of a dynamical evidence accumulation process. Yet within PFC, there is substantial variability in chosen value correlates across individual neurons. Here we show that this variability is explained by neurons having different temporal receptive fields of integration, indexed by examining neuronal spike rate autocorrelation structure whilst at rest. We find that neurons with protracted resting temporal receptive fields exhibit stronger chosen value correlates during choice. Within orbitofrontal cortex, these neurons also sustain coding of chosen value from choice through the delivery of reward, providing a potential neural mechanism for maintaining predictions and updating stored values during learning. These findings reveal that within PFC, variability in temporal specialisation across neurons predicts involvement in specific decision-making computations.

2019 ◽  
Author(s):  
Bhargav Teja Nallapu ◽  
Frédéric Alexandre

AbstractIn the context of flexible and adaptive animal behavior, the orbitofrontal cortex (OFC) is found to be one of the crucial regions in the prefrontal cortex (PFC) influencing the downstream processes of decision-making and learning in the sub-cortical regions. Although OFC has been implicated to be important in a variety of related behavioral processes, the exact mechanisms are unclear, through which the OFC encodes or processes information related to decision-making and learning. Here, we propose a systems-level view of the OFC, positioning it at the nexus of sub-cortical systems and other prefrontal regions. Particularly we focus on one of the most recent implications of neuroscientific evidences regarding the OFC - possible functional dissociation between two of its sub-regions : lateral and medial. We present a system-level computational model of decision-making and learning involving the two sub-regions taking into account their individual roles as commonly implicated in neuroscientific studies. We emphasize on the role of the interactions between the sub-regions within the OFC as well as the role of other sub-cortical structures which form a network with them. We leverage well-known computational architecture of thalamo-cortical basal ganglia loops, accounting for recent experimental findings on monkeys with lateral and medial OFC lesions, performing a 3-arm bandit task. First we replicate the seemingly dissociate effects of lesions to lateral and medial OFC during decision-making as a function of value-difference of the presented options. Further we demonstrate and argue that such an effect is not necessarily due to the dissociate roles of both the subregions, but rather a result of complex temporal dynamics between the interacting networks in which they are involved.Author summaryWe first highlight the role of the Orbitofrontal Cortex (OFC) in value-based decision making and goal-directed behavior in primates. We establish the position of OFC at the intersection of cortical mechanisms and thalamo-basal ganglial circuits. In order to understand possible mechanisms through which the OFC exerts emotional control over behavior, among several other possibilities, we consider the case of dissociate roles of two of its topographical subregions - lateral and medial parts of OFC. We gather predominant roles of each of these sub-regions as suggested by numerous experimental evidences in the form of a system-level computational model that is based on existing neuronal architectures. We argue that besides possible dissociation, there could be possible interaction of these sub-regions within themselves and through other sub-cortical structures, in distinct mechanisms of choice and learning. The computational framework described accounts for experimental data and can be extended to more comprehensive detail of representations required to understand the processes of decision-making, learning and the role of OFC and subsequently the regions of prefrontal cortex in general.


2018 ◽  
Author(s):  
Michael Pereira ◽  
Nathan Faivre ◽  
Iñaki Iturrate ◽  
Marco Wirthlin ◽  
Luana Serafini ◽  
...  

AbstractThe human capacity to compute the likelihood that a decision is correct - known as metacognition - has proven difficult to study in isolation as it usually co-occurs with decision-making. Here, we isolated post-decisional from decisional contributions to metacognition by combining a novel paradigm with multimodal imaging. Healthy volunteers reported their confidence in the accuracy of decisions they made or decisions they observed. We found better metacognitive performance for committed vs. observed decisions, indicating that committing to a decision informs confidence. Relying on concurrent electroencephalography and hemodynamic recordings, we found a common correlate of confidence following committed and observed decisions in the inferior frontal gyrus, and a dissociation in the anterior prefrontal cortex and anterior insula. We discuss these results in light of decisional and post-decisional accounts of confidence, and propose a generative model of confidence in which metacognitive performance naturally improves when evidence accumulation is constrained upon committing a decision.


2020 ◽  
Vol 117 (15) ◽  
pp. 8382-8390 ◽  
Author(s):  
Michael Pereira ◽  
Nathan Faivre ◽  
Iñaki Iturrate ◽  
Marco Wirthlin ◽  
Luana Serafini ◽  
...  

The human capacity to compute the likelihood that a decision is correct—known as metacognition—has proven difficult to study in isolation as it usually cooccurs with decision making. Here, we isolated postdecisional from decisional contributions to metacognition by analyzing neural correlates of confidence with multimodal imaging. Healthy volunteers reported their confidence in the accuracy of decisions they made or decisions they observed. We found better metacognitive performance for committed vs. observed decisions, indicating that committing to a decision may improve confidence. Relying on concurrent electroencephalography and hemodynamic recordings, we found a common correlate of confidence following committed and observed decisions in the inferior frontal gyrus and a dissociation in the anterior prefrontal cortex and anterior insula. We discuss these results in light of decisional and postdecisional accounts of confidence and propose a computational model of confidence in which metacognitive performance naturally improves when evidence accumulation is constrained upon committing a decision.


2018 ◽  
Author(s):  
Arkady Zgonnikov ◽  
Gustav Markkula

Human operators often employ intermittent, discontinuous control strategies in a variety of tasks. A typical intermittent controller monitors control error and generates corrective action when the deviation of the controlled system from the desired state becomes too large to ignore. Most contemporary models of human intermittent control employ simple, threshold-based trigger mechanism to model the process of control activation. However, recent experimental studies demonstrate that the control activation patterns produced by human operators do not support threshold-based models, and provide evidence for more complex activation mechanisms. In this paper, we investigate whether intermittent control activation in humans can be modeled as a decision-making process. We utilize an established drift-diffusion model, which treats decision making as an evidence accumulation process, and study it in simple numerical simulations. We demonstrate that this model robustly replicates the control activation patterns (distributions of control error at movement onset) produced by human operators in previously conducted experiments on virtual inverted pendulum balancing. Our results provide support to the hypothesis that intermittent control activation in human operators can be treated as an evidence accumulation process.


2018 ◽  
Author(s):  
Kitty K. Lui ◽  
Michael D. Nunez ◽  
Jessica M. Cassidy ◽  
Joachim Vandekerckhove ◽  
Steven C. Cramer ◽  
...  

AbstractDecision-making in two-alternative forced choice tasks has several underlying components including stimulus encoding, perceptual categorization, response selection, and response execution. Sequential sampling models of decision-making are based on an evidence accumulation process to a decision boundary. Animal and human studies have focused on perceptual categorization and provide evidence linking brain signals in parietal cortex to the evidence accumulation process. In this exploratory study, we use a task where the dominant contribution to response time is response selection and model the response time data with the drift-diffusion model. EEG measurement during the task show that the Readiness Potential (RP) recorded over motor areas has timing consistent with the evidence accumulation process. The duration of the RP predicts decision-making time, the duration of evidence accumulation, suggesting that the RP partly reflects an evidence accumulation process for response selection in the motor system. Thus, evidence accumulation may be a neural implementation of decision-making processes in both perceptual and motor systems. The contributions of perceptual categorization and response selection to evidence accumulation processes in decision-making tasks can be potentially evaluated by examining the timing of perceptual and motor EEG signals.


2017 ◽  
Author(s):  
Onyekachi Odoemene ◽  
Sashank Pisupati ◽  
Hien Nguyen ◽  
Anne K. Churchland

AbstractThe ability to manipulate neural activity with precision is an asset in uncovering neural circuits for decision-making. Diverse tools for manipulating neurons are available for mice, but the feasibility of mice for decision-making studies remains unclear, especially when decisions require accumulating visual evidence. For example, whether mice’ decisions reflect leaky accumulation is not established, and the relevant and irrelevant factors that influence decisions are unknown. Further, causal circuits for visual evidence accumulation have not been established. To address these issues, we measured >500,000 decisions in 27 mice trained to judge the fluctuating rate of a sequence of flashes. Information throughout the 1000ms trial influenced choice, but early information was most influential. This suggests that information persists in neural circuits for ~1000ms with minimal accumulation leak. Further, while animals primarily based decisions on current stimulus rate, they were unable to entirely suppress additional factors: total stimulus brightness and the previous trial’s outcome. Next, we optogenetically inhibited anteromedial (AM) visual area using JAWS. Importantly, light activation biased choices in both injected and uninjected animals, demonstrating that light alone influences behavior. By varying stimulus-response contingency while holding stimulated hemisphere constant, we surmounted this obstacle to demonstrate that AM suppression biases decisions. By leveraging a large dataset to quantitatively characterize decision-making behavior, we establish mice as suitable for neural circuit manipulation studies, including the one here. Further, by demonstrating that mice accumulate visual evidence, we demonstrate that this strategy for reducing uncertainty in decision-making is employed by animals with diverse visual systems.Significance statementTo connect behaviors to their underlying neural mechanism, a deep understanding of the behavioral strategy is needed. This understanding is incomplete in mouse studies, in part because existing datasets have been too small to quantitatively characterize decision-making behavior. To surmount this, we measured the outcome of over 500,000 decisions made by 27 mice trained to judge visual stimuli. Our analyses offer new insights into mice’ decision-making strategies and compares them with those of other species. We then disrupted neural activity in a candidate neural structure and examined the effect on decisions. Our findings establish mice as a suitable organism for visual accumulation of evidence decisions. Further, the results highlight similarities in decision-making strategies across very different species.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Virginie Fresno ◽  
Shauna L Parkes ◽  
Angélique Faugère ◽  
Etienne Coutureau ◽  
Mathieu Wolff

The ability to flexibly use knowledge is one cardinal feature of goal-directed behaviors. We recently showed that thalamocortical and corticothalamic pathways connecting the medial prefrontal cortex and the mediodorsal thalamus (MD) contribute to adaptive decision-making (Alcaraz et al., 2018). In this study, we examined the impact of disconnecting the MD from its other main cortical target, the orbitofrontal cortex (OFC) in a task assessing outcome devaluation after initial instrumental training and after reversal of action-outcome contingencies. Crossed MD and OFC lesions did not impair instrumental performance. Using the same approach, we found however that disconnecting the OFC from its other main thalamic afferent, the submedius nucleus, produced a specific impairment in adaptive responding following action-outcome reversal. Altogether, this suggests that multiple thalamocortical circuits may act synergistically to achieve behaviorally relevant functions.


2020 ◽  
Author(s):  
Qingfang Liu ◽  
Woojong Yi ◽  
Christian A. Rodriguez ◽  
Samuel M. McClure ◽  
Brandon M. Turner

AbstractIntertemporal choice requires choosing between a smaller reward available after a shorter time delay and a larger reward available after a longer time delay. Previous studies suggest that intertemporal preferences are formed by generating a subjective value of the monetary rewards that depends on reward amount and the associated time delay. Neuroimaging results indicate that this subjective value is tracked by ventral medial prefrontal cortex (vmPFC) and ventral striatum. Subsequently, an accumulation process, subserved by a network including dorsal medial frontal cortex (dmFC), dorsal lateral prefrontal cortex (dlPFC) and posterior parietal cortex (pPC), selects a choice based on the subjective values. The mechanisms of how value accumulation interacts with subjective valuation to make a choice, and how brain regions communicate during decision making are undetermined. We developed and performed an EEG experiment that parametrically manipulated the probability of preferring delayed larger rewards. A computational model equipped with time and reward information transformation, selective attention, and stochastic value accumulation mechanisms was constructed and fit to choice and response time data using a hierarchical Bayesian approach.Phase-based functional connectivity between putative dmFC and pPC was found to be associated with stimulus processing and to resemble the reconstructed accumulation dynamics from the best performing computational model across experimental conditions. By combining computational modeling and phase-based functional connectivity, our results suggest an association between value accumulation, choice competition, and frontoparietal connectivity in intertemporal choice.Author summaryIntertemporal choice is a prominent experimental assay for impulsivity. Behavior in the task involves several cognitive functions including valuation, action selection and self-control. It is unknown how these different functions are temporally implemented during the course of decision making. In the current study, we combined formal computational models of intertemporal choice with a phase-based EEG measure of activity across brain regions to show that functional connectivity between dmFC and pPC reflects cognitive mechanisms of both visual stimulus processing and choice value accumulation. The result supports the notion that dynamic interaction between frontopatietal regions instantiates the critical value accumulation process in intertemporal choice.


2019 ◽  
pp. 17-129
Author(s):  
Edmund T. Rolls

The functioning of the orbitofrontal cortex is described. It is shown that it receives information about what stimulus is present from the sensory pathways, and represents this in terms of its reward value. There are reward outcome neurons (responding to taste and pleasant and unpleasant touch); expected value neurons (responding to visual stimuli according to the expected reward that they predict); and non-reward 'error' neurons that respond when an expected reward is less than expected. There are also neurons that respond to face identity and face expression, and to vocalization. The medial orbitofrontal cortex represents rewards and its activations are related to the pleasantness of stimuli. The lateral orbitofrontal cortex represents punishers and not receiving expected rewards (non-reward). Economic reward value is represented. An anterior region, the ventromedial prefrontal cortex, is implicated in decision-making between rewards of different value. The orbitofrontal cortex represents the reward and punishment value of stimuli, and not actions. Outputs of the orbitofrontal cortex to the cingulate cortex are involved in learning what actions to take to obtain rewards; and to the striatum for stimulus-response, habit, learning.


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