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

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.

Stereotactic electroencephalography in epilepsy patients for mapping of neural circuits related to emotional and psychiatric behaviors: a systematic review

“…27 Within the context of a positive valence domain, high gamma activity in the amygdala was also found to encode outcome value during reward processing. 28 Other authors analyzed amygdala activity via restingstate or naturalistic paradigms to classify neural activity predictive of affective states. 14,16,29,30 Scangos et al examined 24-hour resting-state recordings in 13 patients who were categorized to low-or high-depression groups based on the Patient Health Questionnaire-9 (PHQ-9).…”

“…32,33 High gamma activity in the OFC was observed during outcome valuation, reward prospect, and reward receipt in gambling and subjective choice tasks. 28,[34][35][36] Implementing a monetary incentive delay task, Manssuer et al found that increased OFC and amygdala theta synchronization encoded reward anticipation, whereas amygdala and OFC high gamma activity was observed during monetary loss. 28 In another study, alpha oscillations from the amygdala were found to modulate OFC activity during valence encoding of simple food choices.…”

Clinical neuroscience and neurotechnology: An amazing symbiosis

“…Amygdala electrical stimulation was reported to alter the emotional perception of images ( Bujarski et al., 2021 ), whereas Manssuer et al. identified a network constituted by the amygdala, hippocampus, and the orbitofrontal cortex for reward and loss coding, using a monetary incentive delay task during SEEG recording (used to study the neural correlates of incentive receipt anticipation ( Helfinstein et al., 2013 )) ( Manssuer et al., 2022 ). The orbitofrontal cortex has a role also in decision making ( Saez et al., 2018 ), and emotional processing ( Weisholtz et al., 2022 ).…”

To share or not to share? iEEG evidence for state-dependent inequity encoding in the human OFC

“…The role of the OFC in individual value-based decision-making is well established with converging evidence from lesion, neuroimaging, and electrophysiological studies (Wallis, 2007). The OFC encodes a wide range of valuation-related variables such as probability, reward magnitude, prior expectations, and regret (Camille et al, 2004; Domenech et al, 2020; Manssuer et al, 2022; Padoa-Schioppa & Assad, 2006; Saez et al, 2018). Notably, the medial OFC (mOFC; vmPFC) computes the subjective value (Chib et al, 2009; Hunt et al, 2012; Kable & Glimcher, 2007; Lopez-Persem et al, 2020; Plassmann et al, 2007; Strait et al, 2014).…”