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. 2018 Mar;21(3):415-423.
doi: 10.1038/s41593-018-0082-8. Epub 2018 Feb 19.

Shared neural coding for social hierarchy and reward value in primate amygdala

Jérôme Munuera  1 , Mattia Rigotti  2 , C Daniel Salzman  3   4   5   6   7
Affiliations

Shared neural coding for social hierarchy and reward value in primate amygdala

Jérôme Munuera et al. Nat Neurosci. 2018 Mar.

Abstract

The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank-which contributes to the assessment of the social value of individuals within a group-is linked in the amygdala to representations of rewards associated with nonsocial stimuli.

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Conflict of interest statement

Competing Financial Interests: The authors declare no conflict of interest.

Figures

Figure 1
Figure 1. Task and behavioral measures
A, Sequence of events in behavioral task. Monkeys view images of the faces of other monkeys who reside within their housing room (left panels) or fractal images (right panels). Successful fixation results in reward delivery. B, Behavioral task interleaving social and non-social (fractal) trial blocks. In fractal blocks, different images are associated with different reward amounts, unlike in trials for the social block. C, Social Index from behavioral measures of hierarchical assessment observed during the recording sessions plotted for each viewed monkey, M1 through M8, where M1 is the Alpha monkey and M8 the most submissive one. Kruskal-Wallis test (Chi-sq(7,535)=47.11, p < 1e-07), Dunn’s post-hoc: M1 different from M3 (p = 0.023), M4 (p < 1e-03), M5 (p < 1e-03), M6 (p < 1e-04), M7 (p < 1e-04), M8 (p < 1e-04); M2 vs. M8, p = 0.074). Data represent the average of the 4 behavioral measures used to compute the social index across the sessions (n=17) (see Methods and Supp. Fig. 2). Red diamonds represent mean, white lines represent median, blue bars and whiskers represent 75th and 85th percentiles respectively, blue circles represent data points beyond the whiskers limits. D, Social index score plotted as a function of the scoring of the colony hierarchy by human observer (see Methods, Pearson’s correlation coefficient (two-sided), r = 0.90, p=0.002). E, Index score for each viewer monkey plotted against each other (Pearson’s correlation coefficient (two-sided), r = 0.72, p=0.043).
Figure 2
Figure 2. The amygdala represents the hierarchical status of individuals
A–C. Example neurons from the amygdala (A), OFC (B), and ACC (C) that respond to both face (left panels) and fractal images (right panels). The amygdala neuron responds most strongly to the dominant monkey face image and to the most highly rewarded fractal image, with responses decreasing monotonically with decreases in the hierarchical status of face images or the reward associated with fractals. D. The percentage of neurons in the 3 brain structures that respond to at least one monkey, one fractal or one of both type of images. ** and *** indicate significant differences at p<0.01 and p<0.0001 (two-tailed z-test, top row: amygdala vs. OFC, z = 3.139, p = 0.002; amygdala vs. ACC, z = 4.031, p < 1e-04; OFC vs. ACC, z = 0.614, p = 0.539; middle row: amygdala vs. OFC, z = 1.517, p = 0.129; amygdala vs. ACC, z = 0.855, p = 0.393; OFC vs. ACC, z = −0.723, p = 0.470; bottom row: amygdala vs. OFC, z = 3.126, p = 0.002, amygdala vs. ACC, z = 3.411, p < 1e-03; OFC vs. ACC, z = 0.008, p = 0.994. Analysis have been performed on the entire neuronal population for each brain area: Amygdala, n=196; OFC, n = 134; ACC, n=187; see Methods). E. The proportion of neurons in each brain area that exhibit a significant response to each of the 8 viewed faces. F, Average decoding performance for each brain area for classifying monkey image (left) or fractal (right) identity (n=1000 iterations). Left, curves show the decoding performance for an 8-way classification of monkey face images (equalized number of neurons for the 3 brain areas, n=110 neurons). Right, average decoding performance for each brain structure of discriminating between the 3 fractal images (3-way classifier) (equalized number of neurons for the 3 brain areas, n=131 neurons). Shading, 95% confidence intervals (bootstrap). Dotted lines, chance decoding level. G. Average z-scored firing rate plotted as a function of hierarchical status for neurons that respond more strongly (black line and dots) or weakly (grey line and dots) to a higher ranked monkey (M1) than to a lower ranked monkey (M8) in Amygdala (left panel), OFC (center) and ACC (right). Since neural responses to M1 and M8 are used to classify the cells, these data are excluded from the regression analyses. Pearson’s correlation coefficient (two-sided): amygdala, r = −0.92, p = 0.010, n = 112 neurons (black), r = 0.82, p = 0.046, n = 83 (grey); OFC, r = −0.88, p = 0.021, n = 79 (black), r = −0.32, p = 0.538, n = 49 (grey); ACC, r = 0.19, p = 0.720, n = 97 (black), r = 0.87, p = 0.023, n = 87 (grey). Error bars, SEM. Neural responses were analyzed during the time epoch extending from 100 – 400 ms after image onset for all panels in this figure (fixation was required during this interval).
Figure 3
Figure 3. The same neuronal ensemble in the amygdala can decode reward value and differences in hierarchical status
A, B. Procedure for determining whether same neural ensemble represents the reward associated with fractals and the hierarchical status of viewed face images. A linear decoder is trained to discriminate between fractals associated with large and no reward on a subset of trials (A). Decoding performance was tested on held out fractal trials, or on trials with any two monkey face images (e.g. monkey X and monkey Y) (B). C–E: Decoding performance plotted as a function of time for each brain area when testing the decoder on held-out large and no reward trials. F–H: Decoding performance for each brain area when testing the decoder on high vs. low ranked monkey image trials (M1 vs. M8, i.e. the most distant monkeys in term of social status). I–K: Decoding performance when testing the decoder on two adjacent middle-ranked monkeys (M4 vs. M5). Shading, 95% confidence intervals (bootstrap). Dotted lines, chance decoding level. For all these analyses the decoder has been trained and tested on the entire neuronal population (i.e. no down sampling, n = 1000 iterations, see Methods).
Figure 4
Figure 4. The relationship between the encoding of reward value and hierarchical status
A–C. Peak decoding performance in the amygdala, OFC and ACC tested after training the decoder to classify large vs. no reward trials and testing the decoder for all pairs of monkey face images (e.g. M1 vs. M8, M1 vs. M7, etc., see Methods). Color scale indicates decoding performance minus 0.5, so a value of 0 corresponds to chance decoding. Decoding performance during fixation (100 – 400 ms after image onset), upper left of each plot; decoding performance during free viewing (400–700 ms after image onset), lower right of each plot. D–I, Average decoding performance for each monkey face image (across all comparisons) plotted as a function of that monkey’s social status index for the first (D–F) and second (G–I) time epochs in the 3 brain areas. Note the inversion of sign in the amygdala between the first (D) and second (G) time epochs. For each panel n = 8, Pearson’s correlation coefficient (two-sided): amygdala, r = 0.86, p = 0.006 (1st epoch), r = −0.89, p = 0.003 (2nd epoch); OFC, r = −0.1, p = 0.816 (1st epoch), r = −0.72, p = 0.042 (2nd epoch); ACC, r = 0.42, p = 0.298 (1st epoch), r = 0.47, p = 0.234 (2nd epoch).
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