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

Nature Neurosciencevolume 21pages415423 (2018) | Download Citation

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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Acknowledgements

We thank R. Adolphs, E. Issa and members of the Salzman lab for critical comments on this work and the manuscript. This work was supported by the Fyssen Foundation, Philippe Foundation (J.M), the Simons Foundation and National Institutes of Health grant R01 MH082017 (C.D.S.).

Author information

Affiliations

  1. Department of Neuroscience, Columbia University, New York, NY, USA

    • Jérôme Munuera
    •  & C. Daniel Salzman
  2. IBM T.J. Watson Research Center, Yorktown Heights, NY, USA

    • Mattia Rigotti
  3. Kavli Institute for Brain Sciences, Columbia University, New York, NY, USA

    • C. Daniel Salzman
  4. Department of Psychiatry, Columbia University, New York, NY, USA

    • C. Daniel Salzman
  5. New York State Psychiatric Institute, New York, NY, USA

    • C. Daniel Salzman
  6. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA

    • C. Daniel Salzman

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Contributions

J.M. and C.D.S. designed the study; J.M. performed the experiments; J.M., M.R. and C.D.S. designed analyses; J.M. and M.R. performed analyses; J.M., M.R. and C.D.S. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Jérôme Munuera or C. Daniel Salzman.

Integrated supplementary information

  1. Supplementary Figure 1 Anticipatory licking is correlated with reward magnitude.

    Over the sessions (n=17), the time spent licking during the first 100ms of the trace epoch is plotted for fractals associated with large, low and no reward. Kruskal-Wallis test, Chi-sq(2,48)=25.71, p < 1e-05; Dunn’s post-hoc, Large vs. No Rew., p < 1e-04; Medium vs. No Rew., p = 0.006). 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.

  2. Supplementary Figure 2 Behavioral measures used to compute the social status index.

    A. Trial completion rate; B. The proportion of the time spent viewing the image during the last 333 ms of the free viewing interval; C. The proportion of errors due to fixation break during image presentation; D. The time in which gaze was centered within 3.5 degrees of the center of one of the eyes relative to the time spent viewing other parts of the monkey face during the last 333 ms of the free viewing interval. 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. (n=17 sessions for each box plot; panel B, M5, n = 16 since monkey F made no error for this image during session #15).

  3. Supplementary Figure 3 Social Index from behavioral measures of hierarchical assessment observed during control (unknown monkeys) and main (known monkeys) sessions.

    A. Social Index score of 2 dominant (left bar) and 2 submissive (right bar) unknown monkeys for the viewer monkey (monkey F). No statistical difference between the 2 groups (z=0.4504, p=0.3262, one-tailed Wilcoxon rank sum test). B. Social Index score of 2 dominant (M1 and M2, left bar) and 2 submissive (M7 and M8, right bar) monkeys. These viewed monkeys are members of the same group as the viewer monkey. The 2 groups are statistically different (z=1.8853, p=0.0297, one-tailed Wilcoxon rank sum test). Three equivalent sessions are included for both analyses (n=24 for each box plot, 2 viewed monkeys*4 behavioral measures*3 sessions). 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.

  4. Supplementary Figure 4 Recording locations.

    The location of each neuron is indicated by a '+' on the corresponding coronal slice. Note that a location can contain more than one neuron as several can be recorded on the same channel. Anterior-posterior coordinate of each slice is specified relative to the inter-aural (IA) plane. Diagrams were constructed from anatomical MRIs of each monkey. From left to right: Amygdala, slices 1 and 2 for monkey R and F; ACC, slices 3 and 4 from monkey R, slices 3, 4 and 5 for monkey F; OFC, slices 5 and 6 from monkey R, slices 6 and 7 for monkey F.

  5. Supplementary Figure 5 Amygdala neurons encode information about facial identity.

    A. Single cell PSTH showing a neuron that responded to multiple faces. B. Single cell PSTH showing selectivity for M4 only.

  6. Supplementary Figure 6 Decoding performance is correlated with social distance.

    Average decoding performance in the amygdala when training on fractal images and testing on monkey face images plotted as a function of social distance between the different monkeys in the 1st (A) and 2nd time epochs (B). C. Social distance chart used to compute the social distance between each pair of monkeys ranging from 7 (maximal distance, M1 vs. M8) to 1 (minimal distance M4 vs. M5 or M4 vs. M3, etc). Pearson’s correlation coefficient (two-sided), 1st epoch, r = 0.84, p=0.018; 2nd epoch, r = -0.92, p = 0.003.

  7. Supplementary Figure 7 Correlation between the regression coefficients across the two epochs used for neural analysis.

    A represents the correlation of βfrac, B, represents the correlation of βsoc. Neurons included in these analyses are the ones with a significant (p<0.05) regression factor (β) in either of the 2 intervals. Pearson’s correlation coefficient (two-sided), panel A, n = 94 neurons, r = 0.49, p < 1e-06; panel B, n = 70 neurons r = 0.79, p < 1e-15.

  8. Supplementary Figure 8 Correlation between the two regression coefficients βfrac and βsoc in amygdala, OFC and ACC during the fixation interval (100–400 ms after image onset).

    The correlation coefficients represent the populations that exhibited a correlation with social status ranking (see Fig. 2G; these identified populations were dominant preferring neurons in amygdala (A) and OFC (C) and submissive preferring neurons in amygdala (B) and ACC (D)). Pearson’s correlation coefficient (two-sided): panel A, r = -0.213, p=0.032, n = 102 neurons; B, r = 0.005, p = 0.969, n = 78; C, r = 0.166, p = 0.194, n = 63; D, r = 0.110, p = 0.337, n = 78. Color blue represents the dominant preferring neurons while color red represents the submissive preferring neurons.

  9. Supplementary Figure 9 The relationship between the encoding of reward value and social status in the amygdala.

    A-D. Mean normalized firing plotted for activity during 100 – 400 ms after CS onset for fractal images associated with large, medium and no reward in neuronal populations that exhibited a correlation with social status ranking (see Fig. 2G; these identified populations were dominant preferring neurons in amygdala (A, n= 112 neurons) and OFC (C, n= 79) and submissive preferring neurons in amygdala (B, n= 83 and ACC (D, n= 87). For neurons in the amygdala that responded most strongly to dominant monkey face images (A), the response is significantly stronger (Two-sided paired t-test, t(11) = 2.0306, p = 0.045) to fractals associated with large rewards than to other fractals associated with no reward (Panel B, t(82)=1.2856, p = 0.202; panel C, t(78)=-1.2214, p = 0.226; panel D, t(86)=0.7562, p = 0.452). Red diamonds represent mean, white lines represent median, blue bars and whiskers represent 75th and 98th percentiles respectively, blue dots represent data points beyond the whiskers limits, black dots represent neurons within the 98th percentiles interval.

  10. Supplementary Figure 10 The relationship between the encoding of reward value and social status in the amygdala during the first 300 ms of free viewing epoch (400–700 ms after image onset).

    A. Correlation between the two regression coefficients βfrac and βsoc. Colors represent the dominant preferring neurons (blue points and line), the submissive preferring neurons (red points and line) and all the neurons (black line). Pearson’s correlation coefficient (two-sided): Submissive preferring neurons, r = 0.196, p=0.066, n = 89; Dominant, r = 0.042, p = 0.694, n = 91; All, r = 0.154, p = 0.039, n = 180. B-C. Mean normalized firing plotted for activity during 400 – 700 ms after CS onset for fractal images associated with large, medium and no reward in neuronal populations that exhibited a preference for dominant monkey (B, n=108 neurons) and for submissive monkey (C, n=84 neurons). For neurons in the amygdala that responded most strongly to submissive monkey face images (C), the response is significantly stronger to fractals associated with large rewards than to other fractals associated with no reward (two-sided paired t-test: t(83) = 2.204, p = 0.030). This is not the case for dominant preferring neurons (t(107) = 0.786, p = 0.434). Red diamonds represent mean, white lines represent median, blue bars and whiskers represent 75th and 98th percentiles respectively, blue dots represent data points beyond the whiskers limits, black dots represent neurons within the 98th percentiles interval.

  11. Supplementary Figure 11 The relationship between neural responses to fractals predicting different rewards and face images differing in social rank.

    A-H. Average firing rate of amygdala neurons plotted as a function of time for fractal (Large vs. No Reward) and social (M1/dominant vs. M8/submissive monkey) trials. Neurons were partitioned into groups based on the preference of each neuron for the Large (panels A-B, E-F) or No Reward (panels C-D, G-H) trials in the 1st epoch (100-400ms after FP onset, panels A-D) and 2nd epoch (400-700ms after FP onset, panels E-H) separately (p < 0.05, two-sided unpaired t-test). PSTHs were calculated for these groups for both fractal (left panels) and social trials (right panels). Green curves represent PSTHs of Large Reward Fractal and M1 social trials. Red curves represent PSTHs of No Reward Fractal and M8 social trials. Panels A and B contain the same neurons (n = 47), as do C-D (n=34), E-F (n=37) and G-H (n=25). Shaded area, sem. Window: 50ms, Gaussian kernel.

  12. Supplementary Figure 12 Oculomotor behavior in the fixation interval (100–400 ms after image onset) and the first 300 ms (400–700 ms after image onset) of the free viewing epoch.

    A. The proportion of the time spent viewing the image during the last 300ms of the fixation interval (minimal differences come from eye blinks). B. The proportion of the time spent viewing the image during the first 300ms of the free viewing interval. C. The time in which gaze was centered on the monkey’s eyes relative to the time spent viewing other parts of the social images in the first 300ms of the free viewing epoch. D. The average reaction time of the first saccade after FP extinction in first 300ms of the free viewing epoch. E. The average number of saccades in first 300ms of the free viewing epoch. Red diamonds represent mean, grey lines represent median, blue bars 75th percentiles and whiskers represent 85th (A to C) or 98th (D,E) percentiles, blue circles represent data points beyond the whiskers limits (A,B,C: n=17 sessions; C: n = 2074 trials without eye blinks in this epoch; D: n = 1164 trials with at least 1 saccadic eye movement in this epoch).

  13. Supplementary Figure 13 Oculomotor behavior in the second 300 ms of the free viewing epoch.

    A. The average reaction time of the first saccade (n = 2066 trials without eye blinks in this epoch). B. The average number of saccades. Red diamonds represent mean, grey lines represent median, blue bars and whiskers represent 75th and 98th percentiles respectively, blue circles represent data points beyond the whiskers limits (n = 1175 trials with at least 1 saccadic eye movement in this epoch).

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https://doi.org/10.1038/s41593-018-0082-8