Social reward monitoring and valuation in the macaque brain

Abstract

Behaviors are influenced by rewards to both oneself and others, but the neurons and neural connections that monitor and evaluate rewards in social contexts are unknown. To address this issue, we devised a social Pavlovian conditioning procedure for pairs of monkeys. Despite being constant in amount and probability, the subjective value of forthcoming self-rewards, as indexed by licking and choice behaviors, decreased as partner-reward probability increased. This value modulation was absent when the conspecific partner was replaced by a physical object. Medial prefrontal cortex neurons selectively monitored self-reward and partner-reward information, whereas midbrain dopaminergic neurons integrated this information into a subjective value. Recordings of local field potentials revealed that responses to reward-predictive stimuli in medial prefrontal cortex started before those in dopaminergic midbrain nuclei and that neural information flowed predominantly in a medial prefrontal cortex-to-midbrain direction. These findings delineate a dedicated pathway for subjective reward evaluation in social environments.

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Fig. 1: Emergence of subjective-value difference in social behavioral procedures.
Fig. 2: Nonemergence of subjective value difference in a nonsocial behavioral procedure (monkey S).
Fig. 3: Subjective value coding by dopaminergic neurons.
Fig. 4: Agent-selective reward coding by MPFC neurons.
Fig. 5: Reduction of behavioral and neuronal modulations in nonsocial contexts (monkey S).
Fig. 6: Simultaneous recording of neuronal activity in cortico-subcortical networks.

Data availability:

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

The authors thank M. Ullsperger, A. Fischer, R. Burnside, M. Yoshida, and Y. Kobayashi for their helpful discussions; M. Matsumoto for physiological identification of dopaminergic neurons; and M. Togawa, Y. Yamanishi, and A. Shibata for technical assistance. Japanese monkeys used in this study were provided by the National BioResource Project ‘Japanese Macaques’ of Japan Agency for Medical Research and Development, AMED. This research was supported in part by a Grant-in-Aid for Japan Society for the Promotion of Science KAKENHI (15H04262), the Strategic International Research Cooperative Program from AMED (JP17jm0310011), and the Strategic Research Program for Brain Sciences from AMED (JP18dm0107145) to M.I.

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Contributions

M.I. conceived the experiments. A.N. and M.I. designed and performed the experiments. A.N. analyzed data. A.N. and M.I. wrote the paper. T.N. assisted with data collection and analysis, histology, and manuscript preparation.

Corresponding author

Correspondence to Masaki Isoda.

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Integrated supplementary information

Supplementary Figure 1 Sequence of M1-reward probability during the social Pavlovian procedure.

a, Three possible reward outcomes resulting from behavioral constrains mimicking resource limitation (left) and the number of each outcome for each stimulus (right). Each block consisted of 120 trials and each stimulus was presented equally often (n = 40 trials). b,c, Changes in M1’s reward probability in the self-variable block (b) and the partner-variable block (c). P(M1), M1-reward probability. P(M2), M2-reward probability. P(¬M2), M2-no-reward probability. Note that P(M1) after the outcome to M2 represents the conditional probability of M1’s reward. Grayed areas indicate the stimulus period (1 s) during which the analysis was focused. The numbers in parentheses indicate the number of corresponding cases (see a, right). Detailed account of the probability structure by taking the partner-variable block as an example. In the partner-variable block, three different stimuli were used, that is, stimulus D (P = 0.25 for M2), stimulus E (P = 0.5 for M2), and stimulus F (P = 0.75 for M2), which were presented equally often (each 40 trials; see a, right). Then, the number of trials in which M1 was rewarded was 8 out of the 40 trials for all the stimuli (8/40 = 0.2; see ‘M1-rewarded’ in a, right). Thus, during the stimulus presentation, the reward probability for M1 was, on average, 0.2 ( = 20%) regardless of which stimulus was presented. This is schematically shown in c by using a horizontal line in each stimulus condition with gray backgrounds. Then, there were two different scenarios once the reward outcome for M2 was revealed. The first scenario occurred after M2 was rewarded. The number of trials in which this scenario occurred was 10 for stimulus D, 20 for stimulus E, and 30 for stimulus F (see ‘M2-rewarded’ in a, right). In these trials, M1 was never rewarded; as explained in the main text, there was no trial in which both animals were rewarded on the same trial. Therefore, the conditional probability of M1 to get a reward was 0 ( = 0%; 0/10 for stimulus D, 0/20 for stimulus E, and 0/30 for stimulus F). The second scenario occurred after M2 was unrewarded. The number of trials in which this scenario occurred was 30 for stimulus D, 20 for stimulus E, and 10 for stimulus F (see ‘M1-rewarded’ plus ‘Neither-rewarded’ in a, right;). In these trials, M1 had a chance to receive a reward. Specifically, the conditional probability of M1 to get a reward was, on average, 0.27 (8/30 trials) for stimulus D, 0.4 (8/20 trials) for stimulus E, and 0.8 (8/10 trials) for stimulus F.

Supplementary Figure 2 M1’s gaze behavior in the social Pavlovian procedure.

a, An example of M1’s gaze behavior obtained during a single session (501–1,000 ms after stimulus offset). ROI, region of interest. In the figure, M1 was positioned on the near side (not shown) and M2 was positioned on the far side. b, Proportion of gaze locations entered in the ROI (501–1,000 ms after stimulus offset). **P < 0.01; two-tailed Welch’s t-test. Self-variable block; monkey S, t3519 = 17.32, P = 1.41 × 10−64 (M2 unrewarded, n = 2596 trials; M2 rewarded, n = 649 trials); monkey H, t1390 = 8.1, P = 1.21 × 10−15 (M2 unrewarded, n = 2193 trials; M2 rewarded, n = 550 trials). Partner-variable block; monkey S, t3522 = 5.39, P = 7.61 × 10−8 (M2 unrewarded, n = 1956 trials; M2 rewarded, n = 1974 trials); monkey H, t809 = 3.55, P = 4.07 × 10−4 (M2 unrewarded, n = 1253 trials; M2 rewarded, n = 1253 trials). Red bars, mean. c, A heat map showing the proportion of monkey S’s gaze locations during the stimulus period. Monkey S was positioned on the near side (not shown). Note that this monkey spontaneously looked at the reward-predicting stimuli most of the time, although it was not instructed to do so (see Methods). d, Proportion of monkey S’s gaze locations entered in the ROI during the early and late epochs. Data are plotted for each probability condition. Early, P = 0.68; late, P = 0.47; Spearman rank correlation test (n = 15102, 15112 and 15114 trials for 0.25, 0.50 and 0.75, respectively, in both early and late epochs). The proportion of gaze in the ROI was significantly smaller in the late epoch than in the early epoch (two-tailed paired t-test; t45327 = 32.68, P = 1.5 × 10−231).

Supplementary Figure 3 Lack of subjective-value difference in M2.

M2 did not show differential anticipatory licking behavior in the self-variable block, where M2’s reward probability was the same and M1’s reward probability was variable (see Fig. 1b). Note that M2 received reward outcomes before M1. Monkey B was paired with monkey S, and monkey D was paired with monkey H. **P < 0.01; n.s., not significant (P > 0.8); Spearman rank correlation test. Monkey B: self-variable block, ρ = -3.3 × 10−3, P = 0.88 (n = 690 blocks); partner-variable block, ρ = 0.12, P = 1.37 × 10−7 (n = 690 blocks). Monkey D: self-variable block, ρ = -3.1 × 10−3, P = 0.83 (n = 322 blocks); partner-variable block, ρ = 0.12, P = 2.42 × 10−4 (n = 322 blocks). Center and error bars indicate mean ± s.e.m.

Supplementary Figure 4 Noncontingent social Pavlovian procedure.

a, Four reward outcomes were possible in the noncontingent condition of the social Pavlovian procedure (left). The number of each outcome for each stimulus is shown (right). b,c, No change in M1-reward probability following stimulus offset either in the self-variable block (b) or in the partner-variable block (c). The same conventions are used as in Supplementary Fig. 1. d, Lack of subjective value difference in the partner-variable block when the outcome contingency was absent. The monkeys were first conditioned in the noncontingent condition and then in the contingent condition. **P < 0.01; *P < 0.05; n.s., not significant; Spearman rank correlation test. Center and error bars indicate mean ± s.e.m. Monkey S, contingency (-); self-variable block: ρ = 0.18, P = 5.01 × 10−19 (days 13, n = 2505 trials); ρ = 0.27, P = 1.14 × 10−51 (days 47, n = 3120 trials); partner-variable block: ρ = 0.006, P = 0.76 (days 13, n = 2580 trials); ρ = -7.8 × 10−3, P = 0.66 (days 47, n = 3300 trials). Monkey S, contingency ( + ); self-variable block: ρ = 0.33, P = 1.72 × 10−67 (days 13, n = 2580 trials); ρ= 0.42, P = 4.63 × 10−93 (days 46, n = 2160 trials); partner-variable block: ρ = -0.03, P = 9.19 × 10−2 (days 13, n = 2700 trials); ρ = -5.29 × 10−2, P = 1.39 × 10−2 (days 46, n = 2160 trials). Monkey H, contingency (-); self-variable block: ρ = 6.43 × 10−2, P = 1.7 × 10−3 (days 13, n = 2375 trials); ρ = 0.13, P = 1.39 × 10−13 (days 47, n = 3026 trials); partner-variable block: ρ = 1.38 × 10−2, P = 0.5 (days 13, n = 2383 trials); ρ = 0.3 × 10−3, P = 0.99 (days 47, n = 3336 trials). Monkey H, contingency ( + ); self-variable block: ρ = 0.12, P = 8.71 × 10−4 (days 13, n = 715 trials); ρ = 0.13, P = 0.4 × 10−2 (days 45, n = 479 trials); partner-variable block: ρ = -0.01, P = 0.77 (days 13, n = 716 trials); ρ = -0.2, P = 1.09 × 10−5 (days 45, n = 479 trials).

Supplementary Figure 5 Electrophysiological properties of dopamine neurons.

a, Definition of spike duration. The spike duration was measured from the peak of the first negative component to the peak of the subsequent positive component. b, Distribution of the spike duration for dopaminergic (DA) neurons. Filled red bars indicate dopaminergic neurons with activity that negatively correlated with the partner-reward probability (partner effect). Open black bars indicate dopaminergic neurons without the significant partner effect. For comparison, the spike duration for presumed substantia nigra pars reticulata (SNr) neurons is shown in blue (mean spike duration, 0.23 ms; mean baseline firing rate, 77 Hz; n = 31). c, Baseline firing rate of dopamine neurons was calculated during inter-trial intervals. Values denote the mean and values in parentheses denote s.d. There was no significant difference between neurons with (n = 31 neurons) and without (n = 169 neurons) the significant partner effect in any of the parameters (two-tailed Wilcoxon signed-rank test; firing rate in the self-variable block, P = 0.35; firing rate in the self-variable block, P = 0.11; spike duration, P = 0.45).

Supplementary Figure 6 Subtypes of dopamine neurons.

Scatter plots of sensitivity to the self-reward probability measured in the self-variable block (abscissa) and sensitivity to the partner-reward probability measured in the partner-variable block (ordinate) in the early (left) and late (right) epochs. Each dot represents the data for each neuron (n = 207). The number of each neuronal type is provided in the inset. See Methods for the definition of each neuronal type.

Supplementary Figure 7 Agent-selective MPFC neurons (negative type).

a, Spike density functions for a population of negative self-type MPFC neurons in the early (n = 21 neurons, top) and late (n = 19 neurons, bottom) epochs. b, Spike density functions for a population of negative partner-type MPFC neurons in the early (n = 11 neurons, top) and late (n = 39 neurons, bottom) epochs. Gray rectangles indicate the analysis epochs. See Methods for the definition of positive and negative types.

Supplementary Figure 8 Subjective value measured by choice preference (nonsocial condition).

a, The temporal sequence of events was identical to the procedure shown in Fig. 1d, except that M2’s reward spout was removed. Under this condition, M2 was unable to receive a reward even if the low-pitched tone was presented. b, Choice bias measured for each stimulus pair. The same conventions were used as shown in Fig. 1e. *P < 0.05; **P < 0.01; n.s., not significant; two-tailed paired t-test. Self-variable block (n = 14 blocks for each probability condition): 0.25 vs. 0.5, t13 = 28.88, P = 2.21 × 10−11; 0.25 vs. 0.75, t13 = 173.86, P = 2.84 × 10−23; 0.5 vs. 0.75, t13 = 96.06, P = 6.32 × 10−20. Partner-variable block (n = 13 blocks for each probability condition): 0.25 vs. 0.5, t12 = 5.22 × 10−2, P = 0.96; 0.25 vs. 0.75, t12 = 3.12 × 10−2, P = 0.98; 0.5 vs. 0.75, t12 = 2.6, P = 2.33 × 10−2. Note that the choice bias indicated by * in the partner-variable block is opposite to the choice bias in the social condition (Fig. 1e).

Supplementary Figure 9 Examples of LFP signals recorded in the MPFC.

a, Single-trial raw LFP for each probability condition in the self-variable block (top) and the partner-variable block (bottom). b, Block-averaged LFP for each probability condition in the self-variable block (top) and partner-variable block (bottom). Each probability condition consisted of 40 trials. Note different gains (ordinate) between a and b.

Supplementary Figure 10 Comparison of single-unit spike latencies between dopaminergic neurons and MPFC neurons.

Dopaminergic neurons had a latency basically longer than 100 ms. Approximately 20% of the MPFC neurons had a latency shorter than 100 ms.

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Noritake, A., Ninomiya, T. & Isoda, M. Social reward monitoring and valuation in the macaque brain. Nat Neurosci 21, 1452–1462 (2018). https://doi.org/10.1038/s41593-018-0229-7

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