1 Nature Neuroscience 2012 Vol: 16(2):243-250. DOI: 10.1038/nn.3287

Neuronal reference frames for social decisions in primate frontal cortex

Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.

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Figures
Figure 1: Reward-allocation task.(a) Experimental setup for an actor and a recipient monkey. (b) Stimulus-reward outcome mappings for reward delivered to actor (self), recipient (other) or no one (neither), shown separately for each actor. (c) Magnitude cue used to indicate juice amount at stake for each trial (see d). The position of the horizontal bisecting line specified the percentage of maximum reward that was possible. (d) Task structure (see Online Methods). Top fork, cued trials; bottom fork, choice trials. Dashed gray lines show the angle of the actor's gaze, converging on the fixation point. Eye cartoons indicate times at which the actor could look around. ITI, inter-trial interval; MT, movement time; RT, reaction time. Figure 2: Behavior in the reward-allocation task.(a) Proportions of incomplete trials (mean ± s.e.m.) (see Online Methods) during the reward-allocation task. (b) Choice reaction times (ms) from trials in which rewards were chosen for self, other or neither (mean of session medians ± s.e.m.). (c) Choice preferences (preference index, mean ± s.e.m.) as a function of reward outcome contrasts. Data points next to each bar show the biases for individual sessions. The degree of preference axis on the right shows the range of preference indices in ratio terms. (d) Choice preferences (mean ± s.e.m.) as a function of reward magnitude on 219 single-unit sessions collected with the magnitude cue. Figure 3: Single neurons and population responses from ACCg.(a) Structural magnetic resonance image from actor MO, with example electrode paths for ACCg, ACCs and OFC. cgg, cingulate gyrus; cgs, cingulate sulcus; lofs, lateral orbitofrontal sulcus; mid, midline; mofs, medial orbitofrontal sulcus; ps, principal sulcus. (b) Mean responses (peri-stimulus time histograms, PSTHs) and spike rasters for an other-reward preferring ACCg neuron on choice trials (upper, solid traces) and cued trials (lower, dashed traces). Data are aligned to choice/cue offset (left) and reward onset (right) for each reward outcome. Bar histograms on right show mean ± s.e.m. activity from the two epochs (gray regions). Color codes for PSTH traces and histograms are shown below. (c) PSTHs and spike rasters for a self-reward preferring ACCg neuron. (d) PSTHs and spike rasters for a shared self and other reward–preferring ACCg neuron. (e) Normalized choice/cue epoch and reward epoch responses for 81 ACCg neurons. Data in c–e are presented as in b. In all bar histogram insets, the horizontal lines above different conditions indicate significance differences (black, P < 0.05 by paired t test; green, P < 0.05 by bootstrap test). Figure 4: Single neurons and population responses from ACCs and OFC.(a) PSTHs and spike rasters for a single ACCs neuron preferring forgone rewards. Data are aligned to choice/cue offset (left) and reward onset (right) for each reward outcome. Bar histograms on right show mean ± s.e.m. activity from the two epochs (gray regions). (b) PSTHs and spike rasters for a single OFC neuron preferring self reward. (c) Normalized reward epoch responses of 101 ACCs neurons. (d) Normalized choice/cue epoch and reward epoch responses of 85 OFC neurons. In all panels, data are presented as in Figure 5: Population biases for self, other and neither rewards.(a–c) Scatter plots show mean normalized reward epoch responses (proportion of modulation relative to baseline) of individual neurons (from left to right) between self (self:other) and other rewards, between other and neither rewards, between self rewards from self:neither and self:other contexts, and between self (self:neither) and neither rewards for ACCg (a), ACCs (b) and OFC (c) populations. Regression lines (type II) are shown in red (the circled data points are excluded from the regression). Unity lines are shown in black. The example neurons from Figures 3 and 4 are indicated on the scatter plots. (d) Proportion of neurons (out of significantly classified neurons) from OFC, ACCs and ACCg using self-referenced, other-referenced and both-referenced frames to represent reward outcomes. Inset shows color codes used in the bar graph. Bars indicate significant differences in proportions (P < 0.05, χ2 test). Figure 6: Anatomical projections of recorded locations of all ACCg, ACCs and OFC cells.Recording sites were transformed from chamber coordinates into interaural coordinates. The interaural coordinates of individual cells from both monkeys were then projected onto standard stereotaxic maps of rhesus monkeys50, with a 2-mm interaural spacing in the anterior-posterior dimension. Cells are shown on coronal slices and color-coded for the types of frames of reference used, as specified in Supplementary Table 1 (see box). The lateral view of the brain (inset) shows the locations of the coronal sections. Cd, caudate; cgs, cingulate sulcus; lorb, lateral orbitofrontal sulcus; morb, medial orbitofrontal sulcus; ps, principal sulcus; ros, rostral sulcus. Figure 7: Prosocial behavior and the fidelity of neuronal responses on other:neither trials.(a) ACCg. (b) ACCs. (c) OFC. Coefficients of variation in firing rate (CV; Online Methods) during the reward epoch on other reward trials are plotted as a function of whether actors were more or less prosocial on other:neither trials on the basis of median split (higher: preference index greater than median; lower: preference index less than median). *P < 0.05, bootstrap test.
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References
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    • . . . Critical nodes include ACC9, 10, 11, the OFC12, 13, 14, 15, 16, 17 and subcortical areas, such as the dopaminergic ventral tegmental area, substantia nigra18, 19, the striatum20, 21, the lateral habenula22 and the amygdala23 . . .
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    • . . . Critical nodes include ACC9, 10, 11, the OFC12, 13, 14, 15, 16, 17 and subcortical areas, such as the dopaminergic ventral tegmental area, substantia nigra18, 19, the striatum20, 21, the lateral habenula22 and the amygdala23 . . .
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    • . . . Neuroimaging studies in humans report activation of some of these areas by both giving rewards and receiving rewards24, 25, 26, 27, 28, and lesions to some of these areas result in impaired social decision-making7 . . .
    • . . . In addition, BOLD activity in anterior frontal areas tracks preferences to donate to charity24 . . .
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    • . . . Neuroimaging studies in humans report activation of some of these areas by both giving rewards and receiving rewards24, 25, 26, 27, 28, and lesions to some of these areas result in impaired social decision-making7 . . .
    • . . . These findings suggest that both direct and vicarious reinforcement processes that motivate social decisions are magnified by reward magnitude25, 26, 27. . . .
    • . . . At the population level, neuronal activity selective for allocating rewards to another individual was specific to active decisions (Fig. 3e), similar to what has been reported by functional magnetic resonance imaging of human ventral striatum during voluntary versus forced charitable donations25 . . .
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    • . . . Neuroimaging studies in humans report activation of some of these areas by both giving rewards and receiving rewards24, 25, 26, 27, 28, and lesions to some of these areas result in impaired social decision-making7 . . .
    • . . . These findings suggest that both direct and vicarious reinforcement processes that motivate social decisions are magnified by reward magnitude25, 26, 27. . . .
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    • . . . Neuroimaging studies in humans report activation of some of these areas by both giving rewards and receiving rewards24, 25, 26, 27, 28, and lesions to some of these areas result in impaired social decision-making7 . . .
    • . . . These findings suggest that both direct and vicarious reinforcement processes that motivate social decisions are magnified by reward magnitude25, 26, 27. . . .
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    • . . . Neuroimaging studies in humans report activation of some of these areas by both giving rewards and receiving rewards24, 25, 26, 27, 28, and lesions to some of these areas result in impaired social decision-making7 . . .
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    • . . . Reaction times often serve as a proxy for motivation in incentivized tasks29, 30, 31, 32, 33 . . .
    • . . . Reaction times for making different choices demonstrate that actors discriminated the reward types and had orderly preferences amongst them29, 33 . . .
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    • . . . Reaction times often serve as a proxy for motivation in incentivized tasks29, 30, 31, 32, 33 . . .
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    • . . . Reaction times often serve as a proxy for motivation in incentivized tasks29, 30, 31, 32, 33 . . .
    • . . . The ordered reaction times by monkeys making choices in the reward allocation task suggest that rewarding self is more reinforcing than rewarding the recipient, which is in turn more reinforcing than rewarding no one33. . . .
    • . . . Taken together, these observations support the conclusion that the actor monkeys were acutely aware of the difference between self, other and neither reward outcomes33. . . .
    • . . . Consistent with our previous reports33, 34, actors preferred self rewards over other or neither rewards, but preferred other over neither rewards (Fig. 2c) . . .
    • . . . We previously found that the preference to allocate reward to the other monkey is enhanced by greater familiarity between the two animals and is abolished if the recipient is replaced with a juice collection bottle33 . . .
    • . . . We also observed that reward withholding is reduced when actor monkeys are dominant toward recipients, and that the variability and the degree of preferences often depend on the identity of the recipients33 . . .
    • . . . Furthermore, we found that actor monkeys prefer to deliver juice to themselves than to both themselves and the recipient simultaneously, perhaps reflecting the competitive nature of simultaneously drinking juice, a resource controlled outside of experimental sessions to motivate performance and often monopolized by dominant monkeys living in pairs with subordinate monkeys in their home cages33 (M.L.P., unpublished observation) . . .
    • . . . Furthermore, three pairs could be classified as 'more familiar' with one another because their cages faced each other, as defined previously33 . . .
    • . . . The frequency with which actors looked at recipients was computed from number of gaze shifts to the recipient's face (±8.5° from the center of the face)33, 34 . . .
    • . . . Choice preference indices were constructed as contrast ratios33, 34. . . .
    • . . . Response times, the time from the onset of choices to movement onset, were computed using a 20° s−1 velocity threshold criterion33, 34. . . .
  34. Chang, S.W.; 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) .
    • . . . Consistent with our previous reports33, 34, actors preferred self rewards over other or neither rewards, but preferred other over neither rewards (Fig. 2c) . . .
    • . . . Finally, exogenously increasing oxytocin levels in the CNS amplifies actors' preference to allocate reward to the other monkey over no one34 . . .
    • . . . The frequency with which actors looked at recipients was computed from number of gaze shifts to the recipient's face (±8.5° from the center of the face)33, 34 . . .
    • . . . Choice preference indices were constructed as contrast ratios33, 34. . . .
    • . . . Response times, the time from the onset of choices to movement onset, were computed using a 20° s−1 velocity threshold criterion33, 34. . . .
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    • . . . Furthermore, mirroring of self and other rewards by ACCg neurons is consistent with previous studies linking this area to specifically social functions, such as shared experience and empathy38. . . .
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    • . . . A prior study showed that OFC neurons modulate their activity when a monkey receives juice reward together with another individual39, suggesting that value signals in OFC are sensitive to social context . . .
    • . . . In that study, OFC neurons responded differentially as a function of whether the subject monkey received juice rewards alone or together with another monkey39 . . .
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    • . . . Together, our findings suggest that, as in sensory and motor systems40, identifying the frames of reference in which reward outcomes are encoded may be important for understanding the neural mechanisms underlying social decision-making8. . . .
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    • . . . Furthermore, a group of neurons in the primate medial-frontal cortex selectively responds to observing actions performed by other individuals41 . . .
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    • . . . Accumulating evidence endorses a special role for the medial-frontal cortex in representing information about another individual8, 41, 42, 43, 44 . . .
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    • . . . Accumulating evidence endorses a special role for the medial-frontal cortex in representing information about another individual8, 41, 42, 43, 44 . . .
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    • . . . Accumulating evidence endorses a special role for the medial-frontal cortex in representing information about another individual8, 41, 42, 43, 44 . . .
    • . . . For instance, perceived similarity while observing others is correlated with hemodynamic response in the subgenual ACC44 . . .
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    • . . . Neurons in the dorsolateral prefrontal cortex (DLPFC) track the behavior of a computer opponent in an interactive game45, and BOLD responses in DLPFC and ventromedial prefrontal cortex during observational learning track observed action and observed reward prediction errors, respectively46 . . .
  46. Burke, C.J.; Tobler, P.N.; Baddeley, M.; Schultz, W. Neural mechanisms of observational learning Proc. Natl. Acad. Sci. USA 107, 14431-14436 (2010) .
    • . . . Neurons in the dorsolateral prefrontal cortex (DLPFC) track the behavior of a computer opponent in an interactive game45, and BOLD responses in DLPFC and ventromedial prefrontal cortex during observational learning track observed action and observed reward prediction errors, respectively46 . . .
  47. Hampton, A.N.; Bossaerts, P.; O'Doherty, J.P. Neural correlates of mentalizing-related computations during strategic interactions in humans Proc. Natl. Acad. Sci. USA 105, 6741-6746 (2008) .
    • . . . Brain networks involved in mentalizing47, vicarious pain perception48 and empathy49 therefore seem to be critical for mediating social interactions, suggesting that other-regarding cognition is orchestrated by a distributed network of frontal cortical areas. . . .
  48. Jeon, D. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC Nat. Neurosci. 13, 482-488 (2010) .
    • . . . Brain networks involved in mentalizing47, vicarious pain perception48 and empathy49 therefore seem to be critical for mediating social interactions, suggesting that other-regarding cognition is orchestrated by a distributed network of frontal cortical areas. . . .
  49. Singer, T. Empathy for pain involves the affective but not sensory components of pain Science 303, 1157-1162 (2004) .
    • . . . Brain networks involved in mentalizing47, vicarious pain perception48 and empathy49 therefore seem to be critical for mediating social interactions, suggesting that other-regarding cognition is orchestrated by a distributed network of frontal cortical areas. . . .
  50. Paxinos, G.; Huang, X.F; Toga, A.W. The Rhesus Monkey Brain in Stereotaxic Coordinates , (2000) .
    • . . . The interaural coordinates of individual cells from both monkeys were then projected onto standard stereotaxic maps of rhesus monkeys50, with a 2-mm interaural spacing in the anterior-posterior dimension . . .
  51. Vogt, B.A.; Pandya, D.N. Cingulate cortex of the rhesus monkey. II. Cortical afferents J. Comp. Neurol. 262, 271-289 (1987) .
    • . . . ACCg neurons were recorded from Brodmann areas 24a, 24b and 32, ACCs neurons (dorsal and ventral banks) were recorded from 24c and 24c', and OFC neurons were recorded from 13m and 11 (based on standard anatomical references51, 52; Figs. 3a and 6). . . .
  52. 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) .
    • . . . ACCg neurons were recorded from Brodmann areas 24a, 24b and 32, ACCs neurons (dorsal and ventral banks) were recorded from 24c and 24c', and OFC neurons were recorded from 13m and 11 (based on standard anatomical references51, 52; Figs. 3a and 6). . . .
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