The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys.
A key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both...
Saved in:
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2020-06-01
|
| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3000677&type=printable |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849228269502595072 |
|---|---|
| author | Benjamin M Basile Jamie L Schafroth Chloe L Karaskiewicz Steve W C Chang Elisabeth A Murray |
| author_facet | Benjamin M Basile Jamie L Schafroth Chloe L Karaskiewicz Steve W C Chang Elisabeth A Murray |
| author_sort | Benjamin M Basile |
| collection | DOAJ |
| description | A key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both monkeys, or neither monkey. Here, we assessed whether the ACC's contribution to social cognition is causal by testing rhesus monkeys (Macaca mulatta) on a vicarious reinforcement task before and after they sustained ACC lesions. Prior to surgery, actors learned that 3 different visual cues mapped onto 3 distinct reward outcomes: to self ("Self"), to the other monkey ("Other"), or to neither monkey ("Neither"). On each trial, actors saw a cue that predicted one of the 3 juice offers and could accept the offer by making a saccade to a peripheral target or reject the offer by breaking fixation. Preoperatively, all 6 actors displayed prosocial preferences, indicated by their greater tendency to give reward to Other relative to Neither. Half then received selective, bilateral, excitotoxic lesions of the ACC, and the other half served as unoperated controls. After surgery, all monkeys retained the social preferences they had demonstrated with the preoperatively learned cues, but this preference was reduced in the monkeys with ACC lesions. Critically, none of the monkeys in the ACC lesion group acquired social preferences with a new set of cues introduced after surgery. These data indicate that the primate ACC is necessary for acquisition of prosocial preferences from vicarious reinforcement. |
| format | Article |
| id | doaj-art-fed6789830454c28b693cd80333f3d91 |
| institution | Kabale University |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2020-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-fed6789830454c28b693cd80333f3d912025-08-23T05:30:56ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852020-06-01186e300067710.1371/journal.pbio.3000677The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys.Benjamin M BasileJamie L SchafrothChloe L KaraskiewiczSteve W C ChangElisabeth A MurrayA key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both monkeys, or neither monkey. Here, we assessed whether the ACC's contribution to social cognition is causal by testing rhesus monkeys (Macaca mulatta) on a vicarious reinforcement task before and after they sustained ACC lesions. Prior to surgery, actors learned that 3 different visual cues mapped onto 3 distinct reward outcomes: to self ("Self"), to the other monkey ("Other"), or to neither monkey ("Neither"). On each trial, actors saw a cue that predicted one of the 3 juice offers and could accept the offer by making a saccade to a peripheral target or reject the offer by breaking fixation. Preoperatively, all 6 actors displayed prosocial preferences, indicated by their greater tendency to give reward to Other relative to Neither. Half then received selective, bilateral, excitotoxic lesions of the ACC, and the other half served as unoperated controls. After surgery, all monkeys retained the social preferences they had demonstrated with the preoperatively learned cues, but this preference was reduced in the monkeys with ACC lesions. Critically, none of the monkeys in the ACC lesion group acquired social preferences with a new set of cues introduced after surgery. These data indicate that the primate ACC is necessary for acquisition of prosocial preferences from vicarious reinforcement.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3000677&type=printable |
| spellingShingle | Benjamin M Basile Jamie L Schafroth Chloe L Karaskiewicz Steve W C Chang Elisabeth A Murray The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys. PLoS Biology |
| title | The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys. |
| title_full | The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys. |
| title_fullStr | The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys. |
| title_full_unstemmed | The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys. |
| title_short | The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys. |
| title_sort | anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3000677&type=printable |
| work_keys_str_mv | AT benjaminmbasile theanteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT jamielschafroth theanteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT chloelkaraskiewicz theanteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT stevewcchang theanteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT elisabethamurray theanteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT benjaminmbasile anteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT jamielschafroth anteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT chloelkaraskiewicz anteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT stevewcchang anteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys AT elisabethamurray anteriorcingulatecortexisnecessaryforformingprosocialpreferencesfromvicariousreinforcementinmonkeys |