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Specialized medial prefrontal–amygdala coordination in other-regarding decision preference

Abstract

Social behaviors recruit multiple cognitive operations that require interactions between cortical and subcortical brain regions. Interareal synchrony may facilitate such interactions between cortical and subcortical neural populations. However, it remains unknown how neurons from different nodes in the social brain network interact during social decision-making. Here we investigated oscillatory neuronal interactions between the basolateral amygdala and the rostral anterior cingulate gyrus of the medial prefrontal cortex while monkeys expressed context-dependent positive or negative other-regarding preference (ORP), whereby decisions affected the reward received by another monkey. Synchronization between the two nodes was enhanced for a positive ORP but suppressed for a negative ORP. These interactions occurred in beta and gamma frequency bands depending on the area contributing the spikes, exhibited a specific directionality of information flow associated with a positive ORP and could be used to decode social decisions. These findings suggest that specialized coordination in the medial prefrontal–amygdala network underlies social-decision preferences.

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Fig. 1: Social-reward allocation task and the behaviors associated with social-decision preference.
Fig. 2: Anatomical locations investigated for the coordination of spiking and LFP activity between the BLA and the ACCg.
Fig. 3: Spike–field coherence between the ACCg and the BLA shows frequency-specific and free-choice-selective coordination for positive versus negative ORPs.
Fig. 4: Directionality of information flow between the ACCg and the BLA for positive and negative ORPs as a function of time and frequency.
Fig. 5: Decoding social decisions directly from the spike–field relations between the ACCg and the BLA.

Data availability

Behavioral and neural data presented in this paper are available at https://github.com/changlabneuro/medial-prefrontal-amygdala-coordination-analyses.

Code availability

Behavioral and neural data analysis codes central to this paper are available at https://github.com/changlabneuro/medial-prefrontal-amygdala-coordination-analyses.

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Acknowledgements

We are extremely grateful to B. Pesaran for his guidance on examining oscillatory neural processes throughout the duration of this research. We especially thank D. Lee and A. Kwan for their thoughtful discussions and suggestions on improving this work. We also thank A. Nair and S. Fan for insightful comments on the manuscript. This work was supported by the National Institute of Mental Health (R01MH110750, R01MH120081, R21MH107853 and R00MH099093), the Alfred P. Sloan Foundation (FG-2015-66028) and the Teresa Seessel Postdoctoral Fellowship.

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S.W.C.C. and O.D.M. designed the study and wrote the paper. O.D.M. performed the experiments. C.C.J.C., N.A.F., O.D.M. and S.W.C.C. analyzed the data.

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Correspondence to Steve W. C. Chang.

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Peer review information Nature Neuroscience thanks Ziv Williams and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Figs. 1–11.

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Supplementary Table

Supplementary Table 1. Contains the P values for all the occasions where we use P < 0.05 criterion in the figures (main and supplementary figures) to indicate significant symbols and calculations.

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Dal Monte, O., Chu, C.C.J., Fagan, N.A. et al. Specialized medial prefrontal–amygdala coordination in other-regarding decision preference. Nat Neurosci 23, 565–574 (2020). https://doi.org/10.1038/s41593-020-0593-y

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