Electrophysiological signatures of inequity-dependent reward encoding in the human OFC

Abstract:

Social decision making requires the integration of reward valuation and social cognition systems, both dependent on the orbitofrontal cortex (OFC). How these two OFC functions interact is largely unknown. We recorded intracranial activity from the OFC of ten patients making choices in a social context where reward inequity with a social counterpart varied and could be either advantageous or disadvantageous. We find that OFC high-frequency activity (HFA; 70–150Hz) encodes self-reward, consistent with previous reports. We also observe encoding of the social counterpart’s reward, as well as the type of inequity being experienced. Additionally, we find evidence of inequity-dependent reward encoding: depending on the type of inequity, electrodes rapidly and reversibly switch between different reward-encoding profiles. These results provide direct evidence for encoding of self- and other rewards in the human OFC and highlight the dynamic nature of encoding in the OFC as a function of social context.

Authors:

• Deborah Marciano

• Brooke R. Staveland

• Jack J. Lin

• Ignacio Saez

• Ming Hsu

• Robert T. Knight

Date: 2023

DOI: https://doi.org/10.1016/j.celrep.2023.112865

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Dynamic expectations: Behavioral and electrophysiological evidence of sub-second updates in reward predictions

Abstract:

Expectations are often dynamic: sports fans know that expectations are rapidly updated as games unfold. Yet expectations have traditionally been studied as static. Here we present behavioral and electrophysiological evidence of sub-second changes in expectations using slot machines as a case study. In Study 1, we demonstrate that EEG signal before the slot machine stops varies based on proximity to winning. Study 2 introduces a behavioral paradigm to measure dynamic expectations via betting, and shows that expectation trajectories vary as a function of winning proximity. Notably, these expectation trajectories parallel Study 1’s EEG activity. Studies 3 (EEG) and 4 (behavioral) replicate these findings in the loss domain. These four studies provide compelling evidence that dynamic sub-second updates in expectations can be behaviorally and electrophysiologically measured. Our research opens promising avenues for understanding the dynamic nature of reward expectations and their impact on cognitive processes.

Authors:

• Déborah Marciano

• Ludovic Bellier

• Ida Mayer

• Michael Ruvalcaba

• Sangil Lee

• Ming Hsu

• Robert T. Knight

Date: 2023

DOI: https://doi.org/10.1038/s42003-023-05199-x

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Patients with basal ganglia damage show preserved learning in an economic game

Abstract:

Both basal ganglia (BG) and orbitofrontal cortex (OFC) have been widely implicated in social and non-social decision-making. However, unlike OFC damage, BG pathology is not typically associated with disturbances in social functioning. Here we studied the behavior of patients with focal lesions to either BG or OFC in a multi-strategy competitive game known to engage these regions. We find that whereas OFC patients are significantly impaired, BG patients show intact learning in the economic game. By contrast, when information about the strategic context is absent, both cohorts are significantly impaired. Computational modeling further shows a preserved ability in BG patients to learn by anticipating and responding to the behavior of others using the strategic context. These results suggest that apparently divergent findings on BG contribution to social decision-making may instead reflect a model where higher-order learning processes are dissociable from trial-and-error learning, and can be preserved despite BG damage.

Authors:

• Lusha Zhu

• Yaomin Jiang

• Donatella Scabini

• Robert T. Knight

• Ming Hsu

Date: 2019

DOI: https://doi.org/10.1038/s41467-019-08766-1

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Encoding of multiple reward-related computations in transient and sustained high-frequency activity in human OFC

Abstract:

Human orbitofrontal cortex (OFC) has long been implicated in value-based decision making. In recent years, convergent evidence from human and model organisms has further elucidated its role in representing reward-related computations underlying decision making. However, a detailed description of these processes remains elusive due in part to (1) limitations in our ability to observe human OFC neural dynamics at the timescale of decision processes and (2) methodological and interspecies differences that make it challenging to connect human and animal findings or to resolve discrepancies when they arise. Here, we sought to address these challenges by conducting multi-electrode electrocorticography(ECoG) recordings in neurosurgical patients during economic decision making to elucidate the electrophysiological signature, sub-second temporal profile, and anatomical distribution of reward-related computations within human OFC. We found that high-frequency activity (HFA) (70–200 Hz) reflected multiple valuation components grouped in two classes of valuation signals that were dissociable in temporal profile and information content: (1) fast, transient responses reflecting signals associated with choice and outcome processing, including anticipated risk and outcome regret, and (2) sustained responses explicitly encoding what happened in the immediately preceding trial. Anatomically, these responses were widely distributed in partially overlapping networks, including regions in the central OFC (Brodmann areas 11 and 13), which have been consistently implicated in reward processing in animal single-unit studies. Together, these results integrate insights drawn from human and animal studies and provide evidence for a role of human OFC in representing multiple reward computations.

Authors:

• Ignacio Saez

• Jack Lin

• Arjen Stolk

• Edward Chang

• Josef Parvizi

• Gerwin Schalk

• Robert T. Knight

• Ming Hsu

Date: 2018

DOI: 10.1016/j.cub.2018.07.045

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Damage to dorsolateral prefrontal cortex diminishes the impact of honesty motives on altruistic giving

Authors:

• Lusha Zhu

• Adrianna C. Jenkins

• Eric Set

• Robert T. Knight

• Pearl H. Chiu

• B.R. King-Casas

• Ming Hsu

Date: 2014

DOI: 10.1038/nn.3798

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Abstract:

Substantial correlational evidence suggests that prefrontal regions are critical to honest and dishonest behavior, but causal evidence specifying the nature of this involvement remains absent. We found that lesions of the human dorsolateral prefrontal cortex (DLPFC) decreased the effect of honesty concerns on behavior in economic games that pit honesty motives against self-interest, but did not affect decisions when honesty concerns were absent. These results point to a causal role for DLPFC in honest behavior.