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Functional connectivity between anterior cingulate cortex and orbitofrontal cortex during value-based decision making

https://doi.org/10.1016/j.nlm.2017.11.014Get rights and content

Highlights

  • Reinforcement-guided decision making synchronized neuronal activities in ACC and OFC.

  • Transient rhythmic synchronization between ACC and OFC appeared in low (4–20 Hz) and high (80–100 Hz) frequencies.

  • Low-frequency synchronization during wrongly performed trials was significantly poorer than during correctly performed trials.

Abstract

There is a growing body of evidence showing that the anterior cingulate (ACC) and the orbitofrontal (OFC) cortex are both essential for reinforcement-guided decision making. Focusing on functional connectivity approach through coherence, we studied whether communication between the ACC and OFC through neural synchronization is a necessary stage for performing value-based decision making. We used a T-maze task with a differential reward (Large vs. small reward) and cost (long vs. short waiting time) and simultaneously recorded local field potentials (LFP) from the ACC and OFC. Task-dependent synchronization in theta/low beta (4–20 Hz) frequency bands were observed between areas when rats chose the higher over the lower reward. This synchronization was significantly poorer when rats chose lower rewards or passively performed the task. High-gamma (80–100 Hz) synchrony between areas was also observed, however, it was not dependent on the animal’s decision. Our results propose that synchronization between the ACC and OFC in the low-frequency range is necessary during value-based decision making.

Introduction

Cost-benefit analysis is a weighing and scaling process that everyone performs intuitively at the moment of making any decision by comparing consequences (outcomes) and costs of one’s actions (Rangel, Camerer, & Montague, 2008). A large body of evidence suggests that the anterior cingulate (ACC) and the orbitofrontal cortex (OFC) play important roles in various dimensions of value-based decision making (Khani and Rainer, 2016, Rudebeck et al., 2006, Rushworth et al., 2007). Although, lesion studies in rats and monkeys show that the ACC and OFC process different types of cost (effort vs delay; e.g. Rudebeck et al., 2006), and different choice selection (action vs stimulus; e.g. Rudebeck et al., 2008), electrophysiological studies (e.g. Luk & Wallis, 2013) on both areas represented some degree of overlap between their roles and the results were not as conclusive as lesion studies in suggesting such dissociations. Recently, Khani and Rainer (2016) suggested partially dissociable roles for the ACC and OFC in decision making and the discrepancy between the lesion and electrophysiological studies might result from the functional connectivity of these areas during decision making.

It is now well accepted that the periodic oscillation of neural activity amongst groups of active cells is a fundamental mechanism driving cognitive mechanisms and behaviour (Buzsáki, 2010, Buzsáki and Draguhn, 2004, Fries, 2015). In this scheme, rhythmic excitability in an active network determines the repeated occurrence of a temporal window for communication and thus only coherent oscillatory networks can effectively communicate due to having both input and output windows being open at the same time. Therefore, the presence of such oscillatory coupling enables the communication between the brain regions that are the parts of a dynamic underlying higher cognitive function. Given the existence of rhythmic coupling amongst groups of active cells being reported in human and animal brain during memory (Brincat & Miller, 2015), attention (Saalmann, Pigarev, & Vidyasagar, 2007) and decision making (Neubert, Mars, Sallet, & Rushworth, 2015) tasks, the pathologic oscillation between brain areas has also been reported in a number of neurological conditions such as schizophrenia (McNally & McCarley, 2016) epilepsy (Hughes, 2008) and dyslexia (Vidyasagar, 2013).

If the effective communication amongst cortical areas within a specific timeframe brings about cognitive functions, it is likely to observe oscillatory coupling between brain areas during the course of the task. Given the important of ACC and OFC in different dimensions of decision making, we hypothesized that the activities of both areas become synchronized while animal make the decision to choose the high reward over the low reward at the expense of waiting 15 s to receive the reward. To this end, we simultaneously recorded local field potential (LFP) activities from the ACC and OFC while rats were performing a T-maze paradigm with a different reward.

Section snippets

Animals

Seven male adult Wistar rats were bred in-house at the Neuroscience Research Center, Shahid Beheshti University of Medical Science. Rats caged into groups of two with a 12-h light/dark cycle and access to food and water ad libitum. During the first week, rats were handled and weighed daily. Throughout the experiment, animals were maintained on a restricted diet at 80% of their free-feeding weight but had access to water ad libitum at all times. All experimental procedures were performed

Latency response

The time from poking IR-gate to turning to either arms (latency) was measured for correct (choosing high-reward), error (choosing low-reward) and force trials. Initially, force trials were divided into two groups; match group where animals were forced to choose the arm containing high-reward and non-match group where animals forced to choose arm with low-reward. A t-test was conducted to compare latencies in both groups. There was no significant difference in latencies in match (M = 1457,

Discussion

Our results show neural modulations during reinforcement-guided decision making between two major frontal areas, ACC and OFC. Increased rhythmic oscillation between ACC and OFC in theta, low-beta (4–20 Hz) and also high-gamma (80–100 Hz) suggest that both cortices do play roles in value-based decision making (Jackson, Horst, Pears, Robbins, & Roberts, 2016).

When animals poked the IR-gate, the communication between ACC and OFC increased as it was denoted by an increase in coherence value. This

Acknowledgments

The authors would like to thank the Neuroscience Research Center, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran for all continued support. This work was supported by project grants (No. 808/1392) from the Cognitive Sciences and Technologies Council, Tehran, Iran to AH.

Author contributions

Z.F. Implementing the experimental task and collecting data; A.H. Experiment design, Supervision, Resources, Funding acquisition; A.K. Assist in interpretation of results and preparing the manuscript. M.K. Experiment design, Methodology, Analysis and interpretation of results and writing the manuscript.

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