Reward recalibrates rule representations in human amygdala and hippocampus intracranial recordings

Luis Manssuer (), Qiong Ding, Yashu Feng, Ruoqi Yang, Wei Liu, Bomin Sun, Shikun Zhan () and Valerie Voon ()
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Luis Manssuer: Shanghai Jiao Tong University School of Medicine
Qiong Ding: University of Cambridge
Yashu Feng: Fudan University
Ruoqi Yang: Fudan University
Wei Liu: Shanghai Jiao Tong University School of Medicine
Bomin Sun: Shanghai Jiao Tong University School of Medicine
Shikun Zhan: Shanghai Jiao Tong University School of Medicine
Valerie Voon: Shanghai Jiao Tong University School of Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Adaptive behavior requires the ability to shift responding within (intra-dimensional) or between (extra-dimensional) stimulus dimensions when reward contingencies change. Studies of shifting in humans have focused mainly on the prefrontal cortex and/ or have been restricted to indirect measures of neural activity such as fMRI and lesions. Here, we demonstrate the importance of the amygdala and hippocampus by recording local field potentials directly from these regions intracranially in human epilepsy patients. Reward signals were coded in the high frequency gamma activity (HFG; 60-250 Hz) of both regions and synchronised via low frequency (3-5 Hz) phase-locking only after a shift when patients did not already know the rule and it signalled to stop shifting (“Win-Stay”). In contrast, HFG punishment signals were only seen in the amygdala when the rule then changed and it signalled to start shifting (“Lose-Shift”). During decision-making, hippocampal HFG was more inhibited on non-shift relative to shift trials, suggesting a role in preventing interference in rule representation and amygdala HFG was sensitive to stimulus novelty. The findings expand our understanding of human amygdala-hippocampal function and shifting processes, the disruption of which could contribute to shifting deficits in neuropsychiatric disorders.

Date: 2024
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DOI: 10.1038/s41467-024-53521-w

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