Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

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.

References

  1. Behrens, T. E. J., Hunt, L. T. & Rushworth, M. F. S. The computation of social behavior. Science 324, 1160–1164 (2009).

    CAS  PubMed  Google Scholar 

  2. Bhanji, J. P. & Delgado, M. R. The social brain and reward: social information processing in the human striatum. Wiley Interdiscip. Rev. Cogn. Sci. 5, 61–73 (2014).

    PubMed  Google Scholar 

  3. Sliwa, J. & Freiwald, W. A. A dedicated network for social interaction processing in the primate brain. Science 356, 745–749 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Ruff, C. C. & Fehr, E. The neurobiology of rewards and values in social decision making. Nat. Rev. Neurosci. 15, 549–562 (2014).

    CAS  PubMed  Google Scholar 

  5. Seo, H. & Lee, D. Neural basis of learning and preference during social decision-making. Curr. Opin. Neurobiol. 22, 990–995 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Chang, S. W. C., Gariépy, J.-F. & Platt, M. L. Neuronal reference frames for social decisions in primate frontal cortex. Nat. Neurosci. 16, 243–250 (2013).

    CAS  PubMed  Google Scholar 

  7. Haroush, K. & Williams, Z. M. Neuronal prediction of opponent’s behavior during cooperative social interchange in primates. Cell 160, 1233–1245 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Noritake, A., Ninomiya, T. & Isoda, M. Social reward monitoring and valuation in the macaque brain. Nat. Neurosci. 21, 1452–1462 (2018).

    CAS  PubMed  Google Scholar 

  9. Chang, S. W. C. et al. Neural mechanisms of social decision-making in the primate amygdala. Proc. Natl Acad. Sci. USA 112, 16012–16017 (2015).

    CAS  PubMed  Google Scholar 

  10. Grabenhorst, F., Báez-Mendoza, R., Genest, W., Deco, G. & Schultz, W. Primate amygdala neurons simulate decision processes of social partners. Cell 177, 986–998.e15 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Munuera, J., Rigotti, M. & Salzman, C. D. Shared neural coding for social hierarchy and reward value in primate amygdala. Nat. Neurosci. 21, 415–423 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Azzi, J. C. B., Sirigu, A. & Duhamel, J.-R. Modulation of value representation by social context in the primate orbitofrontal cortex. Proc. Natl Acad. Sci. USA 109, 2126–2131 (2012).

    CAS  Google Scholar 

  13. Baez-Mendoza, R., Harris, C. J. & Schultz, W. Activity of striatal neurons reflects social action and own reward. Proc. Natl Acad. Sci. USA 110, 16634–16639 (2013).

    CAS  PubMed  Google Scholar 

  14. Falcone, R., Brunamonti, E., Ferraina, S. & Genovesio, A. Neural encoding of self and another agent’s goal in the primate prefrontal cortex: human–monkey interactions. Cereb. Cortex 26, 4613–4622 (2016).

    PubMed  Google Scholar 

  15. Nummela, S. U., Jovanovic, V., Mothe, Ldela & Miller, C. T. Social context-dependent activity in marmoset frontal cortex populations during natural conversations. J. Neurosci. 37, 7036–7047 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Apps, M. A. J., Rushworth, M. F. S. & Chang, S. W. C. The anterior cingulate gyrus and social cognition: tracking the motivation of others. Neuron 90, 692–707 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Hill, M. R., Boorman, E. D. & Fried, I. Observational learning computations in neurons of the human anterior cingulate cortex. Nat. Commun. 7, 12722 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Zaki, J. & Ochsner, K. The neuroscience of empathy: progress, pitfalls and promise. Nat. Neurosci. 15, 675–680 (2012).

    CAS  PubMed  Google Scholar 

  19. Mars, R. B. et al. On the relationship between the “default mode network” and the “social brain”. Front. Hum. Neurosci. 6, 189 (2012).

    PubMed  PubMed Central  Google Scholar 

  20. Amadei, E. A. et al. Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles. Nature 546, 297–301 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Allsop, S. A. et al. Corticoamygdala transfer of socially derived information gates observational learning. Cell 173, 1329–1342.e18 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Zhan, Y. et al. Deficient neuron–microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci. 17, 400–406 (2014).

    CAS  PubMed  Google Scholar 

  23. Carmichael, S. T. & Price, J. L. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol. 363, 615–641 (1995).

    CAS  PubMed  Google Scholar 

  24. Klavir, O., Genud-Gabai, R. & Paz, R. Functional connectivity between amygdala and cingulate cortex for adaptive aversive learning. Neuron 80, 1290–1300 (2013).

    CAS  PubMed  Google Scholar 

  25. Pesaran, B. et al. Investigating large-scale brain dynamics using field potential recordings: analysis and interpretation. Nat. Neurosci. 21, 903–919 (2018).

    CAS  PubMed  Google Scholar 

  26. Fries, P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 9, 474–480 (2005).

    PubMed  Google Scholar 

  27. Chang, S. W. C., Winecoff, A. A. & Platt, M. L. Vicarious reinforcement in rhesus macaques (Macaca mulatta). Front. Neurosci. 5, 27 (2011).

    PubMed  PubMed Central  Google Scholar 

  28. Chang, S. W. C., Barter, J. W., Ebitz, R. B., Watson, K. K. & Platt, M. L. Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta). Proc. Natl Acad. Sci. USA 109, 959–964 (2012).

    CAS  PubMed  Google Scholar 

  29. Paxinos, G., Huang, X.-F. & Toga, A. W. The Rhesus Monkey Brain in Stereotaxic Coordinates (Academic Press, 1999).

  30. Baccalá, L. A. & Sameshima, K. Partial directed coherence: a new concept in neural structure determination. Biol. Cybern. 84, 463–474 (2001).

    PubMed  Google Scholar 

  31. Buzsáki, G. & Wang, X.-J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203–225 (2012).

    PubMed  PubMed Central  Google Scholar 

  32. Hipp, J. F., Engel, A. K. & Siegel, M. Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron 69, 387–396 (2011).

    CAS  PubMed  Google Scholar 

  33. Womelsdorf, T., Fries, P., Mitra, P. P. & Desimone, R. Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 439, 733–736 (2006).

    CAS  PubMed  Google Scholar 

  34. Wong, Y. T., Fabiszak, M. M., Novikov, Y., Daw, N. D. & Pesaran, B. Coherent neuronal ensembles are rapidly recruited when making a look-reach decision. Nat. Neurosci. 19, 327–334 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Kahana, M. J., Sekuler, R., Caplan, J. B., Kirschen, M. & Madsen, J. R. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399, 781–784 (1999).

    CAS  PubMed  Google Scholar 

  36. Fujisawa, S. & Buzsáki, G. A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72, 153–165 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Adhikari, A., Topiwala, M. A. & Gordon, J. A. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65, 257–269 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Antzoulatos, E. G. & Miller, E. K. Increases in functional connectivity between prefrontal cortex and striatum during category learning. Neuron 83, 216–225 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Brincat, S. L. & Miller, E. K. Frequency-specific hippocampal–prefrontal interactions during associative learning. Nat. Neurosci. 18, 576–581 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Taub, A. H., Perets, R., Kahana, E. & Paz, R. Oscillations synchronize amygdala-to-prefrontal primate circuits during aversive learning. Neuron 97, 291–298.e3 (2018).

    CAS  PubMed  Google Scholar 

  41. Buschman, T. J. & Miller, E. K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315, 1860–1862 (2007).

    CAS  PubMed  Google Scholar 

  42. Engel, A. K., Fries, P. & Singer, W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2, 704–716 (2001).

    CAS  PubMed  Google Scholar 

  43. Engel, A. K. & Fries, P. Beta-band oscillations—signalling the status quo? Curr. Opin. Neurobiol. 20, 156–165 (2010).

    CAS  PubMed  Google Scholar 

  44. Spitzer, B. & Haegens, S. Beyond the status quo: a role for beta oscillations in endogenous content (re)activation. eNeuro 4, ENEURO.0170-17.2017 (2017).

    PubMed  PubMed Central  Google Scholar 

  45. Cardin, J. A. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663–667 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Jia, X. & Kohn, A. Gamma rhythms in the brain. PLoS Biol. 9, e1001045 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Livneh, U., Resnik, J., Shohat, Y. & Paz, R. Self-monitoring of social facial expressions in the primate amygdala and cingulate cortex. Proc. Natl Acad. Sci. USA 109, 18956–18961 (2012).

    CAS  PubMed  Google Scholar 

  48. Gothard, K. M., Battaglia, F. P., Erickson, C. A., Spitler, K. M. & Amaral, D. G. Neural responses to facial expression and face identity in the monkey amygdala. J. Neurophysiol. 97, 1671–1683 (2007).

    CAS  PubMed  Google Scholar 

  49. Grabenhorst, F., Hernádi, I. & Schultz, W. Prediction of economic choice by primate amygdala neurons. Proc. Natl Acad. Sci. USA 109, 18950–18955 (2012).

    CAS  PubMed  Google Scholar 

  50. Sutton, R. S. & Barto, A. G. Reinforcement Learning: An Introduction (A Bradford Book, 1998).

  51. Liu, Y., Yttri, E. A. & Snyder, L. H. Intention and attention: different functional roles for LIPd and LIPv. Nat. Neurosci. 13, 495–500 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Chung, J. E. et al. A fully automated approach to spike sorting. Neuron 95, 1381–1394.e6 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Bokil, H., Andrews, P., Kulkarni, J. E., Mehta, S. & Mitra, P. P. Chronux: a platform for analyzing neural signals. J. Neurosci. Methods 192, 146–151 (2010).

    PubMed  PubMed Central  Google Scholar 

  54. Bastos, A. M. & Schoffelen, J.-M. A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front. Syst. Neurosci. 9, 175 (2015).

    PubMed  Google Scholar 

  55. Jarvis, M. R. & Mitra, P. P. Sampling properties of the spectrum and coherency of sequences of action potentials. Neural Comput. 13, 717–749 (2001).

    CAS  PubMed  Google Scholar 

  56. Omidvarnia, A. H. et al. Measuring time-varying information flow in scalp EEG signals: orthogonalized partial directed coherence. IEEE Trans. Biomed. Eng. 61, 680–693 (2013).

    PubMed  Google Scholar 

  57. Saez, A., Rigotti, M., Ostojic, S., Fusi, S. & Salzman, C. D. Abstract context representations in primate amygdala and prefrontal cortex. Neuron 87, 869–881 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Steve W. C. Chang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–11.

Reporting Summary

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41593-020-0593-y

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing