scholarly journals Dissociable neural mechanisms track evidence accumulation for selection of attention versus action

2017 ◽  
Author(s):  
Amitai Shenhav ◽  
Mark A. Straccia ◽  
Jonathan D. Cohen ◽  
Matthew M. Botvinick

AbstractDecision-making is typically studied as a sequential process from the selection of what to attend (e.g., between possible tasks, stimuli, or stimulus attributes) to the selection of which actions to take based on the attended information. However, people often gather information across these levels in parallel. For instance, even as they choose their actions, they may continue to evaluate how much to attend other tasks or dimensions of information within a task. We scanned participants while they made such parallel evaluations, simultaneously weighing how much to attend two dynamic stimulus attributes and which response to give based on the attended information. Regions of prefrontal cortex tracked information about the stimulus attributes in dissociable ways, related to either the predicted reward (ventromedial prefrontal cortex) or the degree to which that attribute was being attended (dorsal anterior cingulate, dACC). Within dACC, adjacent regions tracked uncertainty at different levels of the decision, regarding what to attend versus how to respond. These findings bridge research on perceptual and value-based decision-making, demonstrating that people dynamically integrate information in parallel across different levels of decision making.Naturalistic decisions allow an individual to weigh their options within a particular task (e.g., how best to word the introduction to a paper) while also weighing how much to attend other tasks (e.g., responding to e-mails). These different types of decision-making have a hierarchical but reciprocal relationship: Decisions at higher levels inform the focus of attention at lower levels (e.g., whether to select between citations or email addresses) while, at the same time, information at lower levels (e.g., the salience of an incoming email) informs decisions regarding which task to attend. Critically, recent studies suggest that decisions across these levels may occur in parallel, continuously informed by information that is integrated from the environment and from one’s internal milieu1,2.Research on cognitive control and perceptual decision-making has examined how responses are selected when attentional targets are clearly defined (e.g., based on instruction to attend a stimulus dimension), including cases in which responding requires accumulating information regarding a noisy percept (e.g., evidence favoring a left or right response)3-7. Separate research on value-based decision-making has examined how individuals select which stimulus dimension(s) to attend in order to maximize their expected rewards8-11. However, it remains unclear how the accumulation of evidence to select high-level goals and/or attentional targets interacts with the simultaneous accumulation of evidence to select responses according to those goals (e.g., based on the perceptual properties of the stimuli). Recent work has highlighted the importance of such interactions to understanding task selection12-15, multi-attribute decision-making16-18, foraging behavior19-21, cognitive effort22,23, and self-control24-27.While these interactions remain poorly understood, previous research has identified candidate neural mechanisms associated with multi-attribute value-based decision-making11,28,29 and with selecting a response based on noisy information from an instructed attentional target3–5. These research areas have implicated the ventromedial prefrontal cortex (vmPFC) in tracking the value of potential targets of attention (e.g., stimulus attributes)8,11 and the dorsal anterior cingulate cortex (dACC) in tracking an individual’s uncertainty regarding which response to select30–32. It has been further proposed that dACC may differentiate between uncertainty at each of these parallel levels of decision-making (e.g., at the level of task goals or strategies vs. specific motor actions), and that these may be separately encoded at different locations along the dACC’s rostrocaudal axis32,33. However, neural activity within and across these prefrontal regions has not yet been examined in a setting in which information is weighed at both levels within and across trials.Here we use a value-based perceptual decision-making task to examine how people integrate different dynamic sources of information to decide (a) which perceptual attribute to attend and (b) how to respond based on the evidence for that attribute. Participants performed a task in which they regularly faced a conflict between attending the stimulus attribute that offered the greater reward or the attribute that was more perceptually salient (akin to persevering in writing one’s paper when an enticing email awaits). We demonstrate that dACC and vmPFC track evidence for the two attributes in dissociable ways. Across these regions, vmPFC weighs attribute evidence by the reward it predicts and dACC weighs it by its attentional priority (i.e., the degree to which that attribute drives choice). Within dACC, adjacent regions differentiated between uncertainty at the two levels of the decision, regarding what to attend (rostral dACC) versus how to respond (caudal dACC).

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Luca F. Kaiser ◽  
Theo O. J. Gruendler ◽  
Oliver Speck ◽  
Lennart Luettgau ◽  
Gerhard Jocham

AbstractIn a dynamic world, it is essential to decide when to leave an exploited resource. Such patch-leaving decisions involve balancing the cost of moving against the gain expected from the alternative patch. This contrasts with value-guided decisions that typically involve maximizing reward by selecting the current best option. Patterns of neuronal activity pertaining to patch-leaving decisions have been reported in dorsal anterior cingulate cortex (dACC), whereas competition via mutual inhibition in ventromedial prefrontal cortex (vmPFC) is thought to underlie value-guided choice. Here, we show that the balance between cortical excitation and inhibition (E/I balance), measured by the ratio of GABA and glutamate concentrations, plays a dissociable role for the two kinds of decisions. Patch-leaving decision behaviour relates to E/I balance in dACC. In contrast, value-guided decision-making relates to E/I balance in vmPFC. These results support mechanistic accounts of value-guided choice and provide evidence for a role of dACC E/I balance in patch-leaving decisions.


2018 ◽  
Vol 29 (10) ◽  
pp. 4277-4290 ◽  
Author(s):  
Patrick S Hogan ◽  
Joseph K Galaro ◽  
Vikram S Chib

Abstract The perceived effort level of an action shapes everyday decisions. Despite the importance of these perceptions for decision-making, the behavioral and neural representations of the subjective cost of effort are not well understood. While a number of studies have implicated anterior cingulate cortex (ACC) in decisions about effort/reward trade-offs, none have experimentally isolated effort valuation from reward and choice difficulty, a function that is commonly ascribed to this region. We used functional magnetic resonance imaging to monitor brain activity while human participants engaged in uncertain choices for prospective physical effort. Our task was designed to examine effort-based decision-making in the absence of reward and separated from choice difficulty—allowing us to investigate the brain’s role in effort valuation, independent of these other factors. Participants exhibited subjectivity in their decision-making, displaying increased sensitivity to changes in subjective effort as objective effort levels increased. Analysis of blood-oxygenation-level dependent activity revealed that the ventromedial prefrontal cortex (vmPFC) encoded the subjective valuation of prospective effort, and ACC activity was best described by choice difficulty. These results provide insight into the processes responsible for decision-making regarding effort, partly dissociating the roles of vmPFC and ACC in prospective valuation of effort and choice difficulty.


Author(s):  
Benjamin R. Cowley ◽  
Adam C. Snyder ◽  
Katerina Acar ◽  
Ryan C. Williamson ◽  
Byron M. Yu ◽  
...  

AbstractAn animal’s decision depends not only on incoming sensory evidence but also on its fluctuating internal state. This internal state is a product of cognitive factors, such as fatigue, motivation, and arousal, but it is unclear how these factors influence the neural processes that encode the sensory stimulus and form a decision. We discovered that, over the timescale of tens of minutes during a perceptual decision-making task, animals slowly shifted their likelihood of reporting stimulus changes. They did this unprompted by task conditions. We recorded neural population activity from visual area V4 as well as prefrontal cortex, and found that the activity of both areas slowly drifted together with the behavioral fluctuations. We reasoned that such slow fluctuations in behavior could either be due to slow changes in how the sensory stimulus is processed or due to a process that acts independently of sensory processing. By analyzing the recorded activity in conjunction with models of perceptual decision-making, we found evidence for the slow drift in neural activity acting as an impulsivity signal, overriding sensory evidence to dictate the final decision. Overall, this work uncovers an internal state embedded in the population activity across multiple brain areas, hidden from typical trial-averaged analyses and revealed only when considering the passage of time within each experimental session. Knowledge of this cognitive factor was critical in elucidating how sensory signals and the internal state together contribute to the decision-making process.


2021 ◽  
Author(s):  
Payam Piray ◽  
Roshan Cools ◽  
Ivan Toni

Human decisions are known to be strongly influenced by the manner in which options are presented, the "framing effect". Here, we ask whether decision-makers are also influenced by how advice from other knowledgeable agents are framed, a "social framing effect". Concretely, do students learn better from a teacher who often frames advice by emphasizing appetitive outcomes, or do they learn better from another teacher who usually emphasizes avoiding options that can be harmful to their progress? We study the computational and neural mechanisms by which framing of advice affect decision-making, social learning, and trust. We found that human participants are more likely to trust and follow an adviser who often uses an appetitive frame for advice compared with another one who often uses an aversive frame. This social framing effect is implemented through a modulation of the integrative abilities of the ventromedial prefrontal cortex. At the time of choice, this region combines information learned via personal experiences of reward with social information, but the combination differs depending on the social framing of advice. Personally-acquired information is weighted more strongly when dealing with an adviser who uses an aversive frame. The findings suggest that social advice is systematically incorporated into our decisions, while being affected by biases similar to those influencing individual value-based learning.


2017 ◽  
Vol 26 (5) ◽  
pp. 464-469 ◽  
Author(s):  
Dobromir Rahnev

Although most work on perceptual decision making has focused on the processing within the visual, temporal, and parietal lobes, recent research points to an underappreciated but critical role of the prefrontal cortex (PFC). PFC provides high-level control of perception, but it is unclear whether this control can be subdivided into different processes and whether different PFC regions have different roles. Here I review evidence that prefrontal top-down control is organized in the processes of selection control, decision control, and evaluation. These three processes overlap and interact with each other while at the same time maintaining a temporal hierarchy. Further, these different stages are supported by dissociable regions within the PFC that control hierarchically organized cognition. The current proposal for PFC’s role in perceptual control can serve as the basis for a deeper understanding of both the functional organization of PFC and the processes underlying perceptual decision making.


2016 ◽  
Author(s):  
Patrick S. Hogan ◽  
Joseph K. Galaro ◽  
Vikram S. Chib

ABSTRACTThe perceived effort level of an action shapes everyday decisions. Despite the importance of these perceptions for decision-making, the behavioral and neural representations of the subjective cost of effort are not well understood. While a number of studies have implicated anterior cingulate cortex (ACC) in decisions about effort/reward trade-offs, none have experimentally isolated effort valuation from reward and choice difficulty, a function that is commonly ascribed to this region. We used functional magnetic resonance imaging (fMRI) to monitor brain activity while human participants engaged in uncertain choices for prospective physical effort. Our task was designed to examine effort-based decision making in the absence of reward and separated from choice difficulty – allowing us to investigate the brain’s role in effort valuation, independent of these other factors. Participants exhibited subjectivity in their decision-making, displaying increased sensitivity to changes in subjective effort as objective effort levels increased. Analysis of blood-oxygenation level dependent (BOLD) activity revealed that the ventromedial prefrontal cortex (vmPFC) encoded the subjective valuation of prospective effort and ACC encoded choice difficulty. These results provide insight into the processes responsible for decision-making regarding effort, dissociating the roles of vmPFC and ACC in prospective valuation of effort and choice difficulty.


2018 ◽  
Author(s):  
Xiaoxue Gao ◽  
Hongbo Yu ◽  
Ignacio Saez ◽  
Philip R. Blue ◽  
Lusha Zhu ◽  
...  

AbstractHumans are capable of integrating social contextual information into decision-making processes to adjust their attitudes towards inequity. This context-dependency emerges both when individual is better off (i.e. advantageous inequity) and worse off (i.e. disadvantageous inequity) than others. It is not clear however, whether the context-dependent processing of advantageous and disadvantageous inequity rely on dissociable or shared neural mechanisms. Here, by combining an interpersonal interactive game that gave rise to interpersonal guilt and different versions of the dictator games that enabled us to characterize individual weights on aversion to advantageous and disadvantageous inequity, we investigated the neural mechanisms underlying the two forms of inequity aversion in the interpersonal guilt context. In each round, participants played a dot-estimation task with an anonymous co-player. The co-players received pain stimulation with 50% probability when anyone responded incorrectly. At the end of each round, participants completed a dictator game, which determined payoffs of him/herself and the co-player. Both computational model-based and model-free analyses demonstrated that when inflicting pain upon co-players (i.e., the guilt context), participants cared more about advantageous inequity and became less sensitive to disadvantageous inequity, compared with other social contexts. The contextual effects on two forms of inequity aversion are uncorrelated with each other at the behavioral level. Neuroimaging results revealed that the context-dependent representation of inequity aversion exhibited a spatial gradient in activity within the insula, with anterior parts predominantly involved in the aversion to advantageous inequity and posterior parts predominantly involved in the aversion to disadvantageous inequity. The dissociable mechanisms underlying the two forms of inequity aversion are further supported by the involvement of right dorsolateral prefrontal cortex and dorsomedial prefrontal cortex in advantageous inequity processing, and the involvement of right amygdala and dorsal anterior cingulate cortex in disadvantageous inequity processing. These results extended our understanding of decision-making processes involving inequity and the social functions of inequity aversion.


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