Repository logo
 

Integrated Amygdala, Orbitofrontal and Hippocampal Contributions to Reward and Loss Coding Revealed with Human Intracranial EEG

Published version
Peer-reviewed

Loading...
Thumbnail Image

Type

Article

Change log

Authors

Manssuer, Luis 
Ding, Qiong 
Liu, Wei 
Ruoqi, Yang 
Linbin, Wang 

Abstract

Neurophysiological work in primates and rodents have shown the amygdala plays a central role in reward processing through connectivity with the orbitofrontal cortex (OFC) and hippocampus. However, understanding the role of oscillations in each region and their connectivity in different stages of reward processing in humans has been hampered by limitations with non-invasive methods such as poor spatial and temporal resolution. To overcome these limitations, we recorded local field potentials (LFPs) directly from the amygdala, OFC and hippocampus simultaneously in human male and female epilepsy patients performing a monetary incentive delay task. This allowed us to dissociate electrophysiological activity and connectivity patterns related to the anticipation and receipt of rewards and losses in real-time. Anticipation of reward increased high frequency gamma (HFG) (60-250 Hz) activity in the hippocampus and theta band (4-8 Hz) synchronization between amygdala and OFC, suggesting roles in memory and motivation. During receipt, HFG in the amygdala was involved in outcome value coding, the OFC cue context-specific outcome value comparison and the hippocampus reward coding. Receipt of loss decreased amygdala-hippocampus theta and increased amygdala-OFC HFG amplitude coupling which coincided with subsequent adjustments in behaviour. Increased HFG synchronization between the amygdala and hippocampus during reward receipt suggested encoding of reward information into memory for reinstatement during anticipation. These findings extend what is known about the primate brain to humans, showing key spectrotemporal coding and communication dynamics for reward and punishment related processes which could serve as more precise targets for neuromodulation to establish causality and potential therapeutic applications.

Description

Keywords

IEEG, OFC, amygdala, connectivity, reward, value, Amygdala, Animals, Electrocorticography, Female, Hippocampus, Humans, Male, Motivation, Prefrontal Cortex, Reward

Journal Title

The Journal of Neuroscience

Conference Name

Journal ISSN

0270-6474
1529-2401

Volume Title

Publisher

Society for Neuroscience
Sponsorship
Medical Research Council (MR/P008747/1)
Natural Science Foundation of China grant (81771482) to BMS. SJTU Trans-med Awards Research (2019015) to BMS. Shanghai Clinical Research Centre for Mental Health (19MC191100) to BMS. Medical Research Council Senior Clinical Fellowship (Grant No. MR/P008747/1) to VV.