Neuronal correlates of strategic cooperation in monkeys

Abstract

We recorded neural activity in male monkeys playing a variant of the game ‘chicken’ in which they made decisions to cooperate or not cooperate to obtain rewards of different sizes. Neurons in the middle superior temporal sulcus (mSTS)—previously implicated in social perception—signaled strategic information, including payoffs, intentions of the other player, reward outcomes and predictions about the other player. Moreover, a subpopulation of mSTS neurons selectively signaled cooperatively obtained rewards. Neurons in the anterior cingulate gyrus, previously implicated in vicarious reinforcement and empathy, carried less information about strategic variables, especially cooperative reward. Strategic signals were not reducible to perceptual information about the other player or motor contingencies. These findings suggest that the capacity to compute models of other agents has deep roots in the strategic social behavior of primates and that the anterior cingulate gyrus and the mSTS support these computations.

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Fig. 1: Modified chicken game with the option to cooperate.
Fig. 2: Monkeys understand the task and discriminate social context.
Fig. 3: Monkey choice behavior is best explained by a sophisticated, recursive model including information about payoffs for self and other, other player’s predicted strategy and SPE.
Fig. 4: Example mSTS neuron signaling cooperative reward independent of gaze direction and reward size.
Fig. 5: Example ACCg neuron sensitive to cooperative reward independent of gaze direction and reward size.
Fig. 6: Neurons in the ACCg and the mSTS signal strategic information.
Fig. 7: Strategic signaling by mSTS neurons is independent of visual responsiveness and feature selectivity.

Data availability

The data forming the basis of this study are available from the corresponding author upon reasonable request.

Code availability

The custom analysis code used in this study is available from the corresponding author upon reasonable request.

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Acknowledgements

We thank the members of Duke University’s Division of Laboratory Animal Resources for their superb animal care. This work was supported by a grant from SFARI (304935, to M.L.P.), and by R01 MH095894, R01 NS088674, R37 MH109728 and R01 MH108627.

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Authors

Contributions

W.S.O. conceived and carried out the experiments and analyzed the data. S.M.-K. designed the strategic learning model. W.S.O. and M.L.P. wrote the manuscript with input from S.M.-K.

Corresponding author

Correspondence to Wei Song Ong.

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The authors declare no competing interests.

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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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Extended data

Extended Data Fig. 1 Monitoring of gaze behavior and trial outcomes.

a, ROIs for M1’s gaze (red) indicated by rectangles drawn around other monkey’s face, other player’s car, and the payout tokens ahead and to the side. All other gaze points directed to the screen are labeled ‘Screen’. b, Proportion of trials resulting in mixed strategy Nash equilibrium when Vstr>Vcoop and pure Nash equilibrium when Vcoop>Vstr. Solid light blue line, high joystick direction signal (90% dot motion coherence) trials; dotted dark blue line, ambiguous joystick direction signal (0% dot motion coherence) trials. Fine lines indicate + - SEM for 4 live monkey pairs (n = 75,630 trials). c, Monkeys look at the most informative stimuli, calibrated by social context. Top panel: Probability M1 looked towards other player’s car (i) or face/face space (computer condition) (ii), aligned to moving dots onset, in live (blue), decoy (green), and computer (black) conditions. Bottom panel: Difference in probability of gaze towards other player’s car (i) or face (ii) on high and ambiguous joystick direction signal (dot motion coherence) trials. All data calculated in 1 ms bins.

Extended Data Fig. 2 Choice outcomes over time and between agency conditions, and the effect of dominance relationships on model fits.

a, Probability of a crash (top panel) or cooperate (lower panel) event over time. Each point represents a bin of 5 trials from all sessions as a function of social context (blue, live; green, decoy; gray, computer. n = 164,259 trials). b, Probability of a crash (top panel) or cooperate (lower panel) event as a function of payout conditions (difference in the number of tokens available straight ahead, Vstr, and cooperate, Vcoop). Red circles/solid lines, high joystick direction signal (90% dot motion coherence) trials; black triangles/dashed lines, ambiguous joystick direction signal (0% dot motion coherence) trials. c, Frequency of deviating as a function of frequency of choosing straight for 4 monkey pairs, segregated by social dominance. For a given pair, number of times they chose deviate (y-axis) or straight (x-axis) are plotted. Symbol fill colors indicate monkey identity; symbol outline colors indicate monkey dyads. Note that mid-ranking monkeys (purple and brown) fall on both sides of the diagonal, suggesting that strategy depends more on relative status than identity. d, Improvements in model fits depend on dominance relationship between monkeys. Models were fit to each monkey’s choices playing specific other monkeys. Y-axis shows increase in AIC/trial when intention was added to model. Within each monkey pair, one was always dominant to the other, and AIC/trials are segregated by relative status. Grey dotted lines connect monkeys playing each other; colors indicate monkey identity.

Extended Data Fig. 3 Location of neural recordings (ACCg & mSTS) and example neurons.

a, Recording locations in ACCg (orange, coronal section) and mSTS (green, coronal and para-sagittal sections). CS, cingulate sulcus; LS, lateral sulcus; A, anterior; P, posterior. A/P distance from inter-aural 0 indicated for coronal sections. b, PSTHs for 2 example ACCg neurons and 2 example mSTS neurons in monkeys playing a live monkey, aligned to moving dots onset (left) and juice delivery (right). Payoff token onset occurs 500 ms before dots onset, cars move 4 s, later and juice delivery occurs 900 ± 100 ms after cars move. Top two rows, example neurons sensitive to payouts (light blue: Vstraight > Vcooperate; dark blue: Vcooperate > Vstraight); bottom two rows, neurons sensitive to joystick direction signal strength (dot motion coherence); dark red, 0% coherence; light red, 90% coherence.

Supplementary information

Supplementary Information

Supplementary Figs. 1–5 and Supplementary Tables 1–6.

Reporting Summary

Supplementary Video

Task video showing two players performing the task, with outcomes indicated in the box below and eyetracking of player 1 (yellow dot).

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Ong, W.S., Madlon-Kay, S. & Platt, M.L. Neuronal correlates of strategic cooperation in monkeys. Nat Neurosci 24, 116–128 (2021). https://doi.org/10.1038/s41593-020-00746-9

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