scholarly journals Interaction between decision-making and interoceptive representations of bodily arousal in frontal cortex

2021 ◽  
Vol 118 (35) ◽  
pp. e2014781118
Author(s):  
Atsushi Fujimoto ◽  
Elisabeth A. Murray ◽  
Peter H. Rudebeck

Decision-making and representations of arousal are intimately linked. Behavioral investigations have classically shown that either too little or too much bodily arousal is detrimental to decision-making, indicating that there is an inverted “U” relationship between bodily arousal and performance. How these processes interact at the level of single neurons as well as the neural circuits involved are unclear. Here we recorded neural activity from orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaque monkeys while they made reward-guided decisions. Heart rate (HR) was also recorded and used as a proxy for bodily arousal. Recordings were made both before and after subjects received excitotoxic lesions of the bilateral amygdala. In intact monkeys, higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and dACC selectively encoded trial-by-trial variations in HR independent of reward value. After amygdala lesions, HR increased, and the relationship between HR and RTs was altered. Concurrent with this change, there was an increase in the proportion of dACC neurons encoding HR. Applying a population-coding analysis, we show that after bilateral amygdala lesions, the balance of encoding in dACC is skewed away from signaling either reward value or choice direction toward HR coding around the time that choices are made. Taken together, the present results provide insight into how bodily arousal and decision-making are signaled in frontal cortex.

2021 ◽  
Author(s):  
Atsushi Fujimoto ◽  
Elisabeth A. Murray ◽  
Peter H. Rudebeck

AbstractDecision-making and representations of arousal are intimately linked. Behavioral investigations have classically shown that either too little or too much bodily arousal is detrimental to decision-making, indicating that there is an inverted ‘U’ relationship between bodily arousal and performance. How these processes interact at the level of single neurons as well as the neural circuits involved are unclear. Here we recorded neural activity from orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaque monkeys while they made reward-guided decisions. Heart rate (HR) was also recorded as a proxy for bodily arousal. Recordings were made both before and after subjects received excitotoxic lesions of the bilateral amygdala. In intact monkeys, higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and dACC selectively encoded trial-by-trial variations in HR independent of reward value. After amygdala lesions, HR increased and the relationship between HR and RTs was reversed. Concurrent with this change, there was an increase in the proportion of dACC neurons encoding HR. Applying a novel population-coding analysis, we show that bilateral amygdala lesions skew the balance of encoding in dACC away from signaling either reward value or choice direction towards HR coding around the time that choices are made. Taken together, the present results provide insight into how bodily arousal and decision-making are signaled in frontal cortex. Our findings may shed light on the neural mechanisms underlying some psychiatric disorders linked to amygdala dysfunction that are characterized by heightened arousal and deficits in decision-making.Significance statementHow bodily arousal states influence decision-making has been a central question in psychology, but the neural mechanisms are unclear. We recorded heart rate, a measure of bodily arousal, while simultaneously monitoring neural activity in orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaques making reward-guided decisions. In intact macaques higher HR was associated with shorter reaction times. Concurrently, the activity of a set of neurons in OFC and dACC selectively encoded HR. Following amygdala lesions, HR generally increased and now the relationship between HR and reaction times was reversed. At the neural level, the balance of encoding in dACC shifted towards signaling HR, suggesting a specific mechanism through which arousal influences decision-making.


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.


2019 ◽  
Author(s):  
Luc Vermeylen ◽  
David Wisniewski ◽  
Carlos González-García ◽  
Vincent Hoofs ◽  
Wim Notebaert ◽  
...  

AbstractInfluential theories of medial frontal cortex (MFC) function suggest that the MFC registers cognitive conflict as an aversive signal, but no study directly tested this idea. Instead, recent studies suggested that non-overlapping regions in the MFC process conflict and affect. In this pre-registered human fMRI study, we used multivariate pattern analyses to identify which regions respond similarly to conflict and aversive signals. The results reveal that, of all conflict- and value-related regions, the ventral pre-supplementary motor area (or dorsal anterior cingulate cortex) showed a shared neural pattern response to different conflict and affect tasks. These findings challenge recent conclusions that conflict and affect are processed independently, and provide support for integrative views of MFC function.


2018 ◽  
Vol 115 (33) ◽  
pp. E7680-E7689 ◽  
Author(s):  
Xiaoxue Gao ◽  
Hongbo Yu ◽  
Ignacio Sáez ◽  
Philip R. Blue ◽  
Lusha Zhu ◽  
...  

Humans can integrate social contextual information into decision-making processes to adjust their responses toward inequity. This context dependency emerges when individuals receive more (i.e., advantageous inequity) or less (i.e., disadvantageous inequity) than others. However, it is not clear whether context-dependent processing of advantageous and disadvantageous inequity involves differential neurocognitive mechanisms. Here, we used fMRI to address this question by combining an interactive game that modulates social contexts (e.g., interpersonal guilt) with computational models that enable us to characterize individual weights on inequity aversion. In each round, the participant played a dot estimation task with an anonymous coplayer. The coplayer would receive pain stimulation with 50% probability when either of them responded incorrectly. At the end of each round, the participant completed a variant of dictator game, which determined payoffs for him/herself and the coplayer. Computational modeling demonstrated the context dependency of inequity aversion: when causing pain to the coplayer (i.e., guilt context), participants cared more about the advantageous inequity and became more tolerant of the disadvantageous inequity, compared with other conditions. Consistently, neuroimaging results suggested the two types of inequity were associated with differential neurocognitive substrates. While the context-dependent processing of advantageous inequity was associated with social- and mentalizing-related processes, involving left anterior insula, right dorsolateral prefrontal cortex, and dorsomedial prefrontal cortex, the context-dependent processing of disadvantageous inequity was primarily associated with emotion- and conflict-related processes, involving left posterior insula, right amygdala, and dorsal anterior cingulate cortex. These results extend our understanding of decision-making processes related to inequity aversion.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Karima Chakroun ◽  
David Mathar ◽  
Antonius Wiehler ◽  
Florian Ganzer ◽  
Jan Peters

Involvement of dopamine in regulating exploration during decision-making has long been hypothesized, but direct causal evidence in humans is still lacking. Here, we use a combination of computational modeling, pharmacological intervention and functional magnetic resonance imaging to address this issue. Thirty-one healthy male participants performed a restless four-armed bandit task in a within-subjects design under three drug conditions: 150 mg of the dopamine precursor L-dopa, 2 mg of the D2 receptor antagonist haloperidol, and placebo. Choices were best explained by an extension of an established Bayesian learning model accounting for perseveration, directed exploration and random exploration. Modeling revealed attenuated directed exploration under L-dopa, while neural signatures of exploration, exploitation and prediction error were unaffected. Instead, L-dopa attenuated neural representations of overall uncertainty in insula and dorsal anterior cingulate cortex. Our results highlight the computational role of these regions in exploration and suggest that dopamine modulates how this circuit tracks accumulating uncertainty during decision-making.


2017 ◽  
Vol 48 (2) ◽  
pp. 327-336 ◽  
Author(s):  
O. T. Ousdal ◽  
Q. J. Huys ◽  
A. M. Milde ◽  
A. R. Craven ◽  
L. Ersland ◽  
...  

BackgroundDisturbances in Pavlovian valuation systems are reported to follow traumatic stress exposure. However, motivated decisions are also guided by instrumental mechanisms, but to date the effect of traumatic stress on these instrumental systems remain poorly investigated. Here, we examine whether a single episode of severe traumatic stress influences flexible instrumental decisions through an impact on a Pavlovian system.MethodsTwenty-six survivors of the 2011 Norwegian terror attack and 30 matched control subjects performed an instrumental learning task in which Pavlovian and instrumental associations promoted congruent or conflicting responses. We used reinforcement learning models to infer how traumatic stress affected learning and decision-making. Based on the importance of dorsal anterior cingulate cortex (dACC) for cognitive control, we also investigated if individual concentrations of Glx (=glutamate + glutamine) in dACC predicted the Pavlovian bias of choice.ResultsSurvivors of traumatic stress expressed a greater Pavlovian interference with instrumental action selection and had significantly lower levels of Glx in the dACC. Across subjects, the degree of Pavlovian interference was negatively associated with dACC Glx concentrations.ConclusionsExperiencing traumatic stress appears to render instrumental decisions less flexible by increasing the susceptibility to Pavlovian influences. An observed association between prefrontal glutamatergic levels and this Pavlovian bias provides novel insight into the neurochemical basis of decision-making, and suggests a mechanism by which traumatic stress can impair flexible instrumental behaviours.


2001 ◽  
Vol 99 (1) ◽  
pp. 523-528 ◽  
Author(s):  
G. Bush ◽  
B. A. Vogt ◽  
J. Holmes ◽  
A. M. Dale ◽  
D. Greve ◽  
...  

2021 ◽  
pp. 1-10
Author(s):  
Megan E. Monko ◽  
Sarah R. Heilbronner

Abstract Previous studies of the retrosplenial cortex (RSC) have focused on its role in navigation and memory, consistent with its well-established medial temporal connections, but recent evidence also suggests a role for this region in reward and decision making. Because function is determined largely by anatomical connections, and to better understand the anatomy of RSC, we used tract-tracing methods to examine the anatomical connectivity between the rat RSC and frontostriatal networks (canonical reward and decision-making circuits). We find that, among frontal cortical regions, RSC bidirectionally connects most strongly with the anterior cingulate cortex, but also with an area of the central–medial orbito-frontal cortex. RSC projects to the dorsomedial striatum, and its terminal fields are virtually encompassed by the frontal-striatal projection zone, suggestive of functional convergence through the basal ganglia. This overlap is driven by anterior cingulate cortex, prelimbic cortex, and orbito-frontal cortex, all of which contribute to goal-directed decision making, suggesting that the RSC is involved in similar processes.


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