A Frontopolar-temporal Circuit Determines the Impact of Social Information in Macaque Decision Making

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2023 Oct 20

PMID 37863039

Authors

Ali Mahmoodi

Caroline Harbison

Alessandro Bongioanni

Andrew Emberton

Lea Roumazeilles

Jerome Sallet

Nima Khalighinejad

Matthew F S Rushworth

Affiliations

Soon will be listed here.

Abstract

When choosing, primates are guided not only by personal experience of objects but also by social information such as others' attitudes toward the objects. Crucially, both sources of information-personal and socially derived-vary in reliability. To choose optimally, one must sometimes override choice guidance by personal experience and follow social cues instead, and sometimes one must do the opposite. The dorsomedial frontopolar cortex (dmFPC) tracks reliability of social information and determines whether it will be attended to guide behavior. To do this, dmFPC activity enters specific patterns of interaction with a region in the mid-superior temporal sulcus (mSTS). Reversible disruption of dmFPC activity with transcranial ultrasound stimulation (TUS) led macaques to fail to be guided by social information when it was reliable but to be more likely to use it when it was unreliable. By contrast, mSTS disruption uniformly downregulated the impact of social information on behavior.

Citing Articles

Transcranial ultrasound stimulation effect in the redundant and synergistic networks consistent across macaques.

Gatica M, Atkinson-Clement C, Mediano P, Alkhawashki M, Ross J, Sallet J Netw Neurosci. 2024; 8(4):1032-1050.

PMID: 39735508 PMC: 11674579. DOI: 10.1162/netn_a_00388.

Causal involvement of dorsomedial prefrontal cortex in learning the predictability of observable actions.

Kang P, Moisa M, Lindstrom B, Soutschek A, Ruff C, Tobler P Nat Commun. 2024; 15(1):8305.

PMID: 39333062 PMC: 11436984. DOI: 10.1038/s41467-024-52559-0.

Ventral frontostriatal circuitry mediates the computation of reinforcement from symbolic gains and losses.

Tang H, Bartolo R, Averbeck B Neuron. 2024; 112(22):3782-3795.e5.

PMID: 39321792 PMC: 11581918. DOI: 10.1016/j.neuron.2024.08.018.

Lesions to the mediodorsal thalamus, but not orbitofrontal cortex, enhance volatility beliefs linked to paranoia.

Suthaharan P, Thompson S, Rossi-Goldthorpe R, Rudebeck P, Walton M, Chakraborty S Cell Rep. 2024; 43(6):114355.

PMID: 38870010 PMC: 11231991. DOI: 10.1016/j.celrep.2024.114355.

References

Wardak C, Vanduffel W, Orban G . Searching for a salient target involves frontal regions. Cereb Cortex. 2010; 20(10):2464-77. DOI: 10.1093/cercor/bhp315. View

Mahmoodi A, Bang D, Olsen K, Zhao Y, Shi Z, Broberg K . Equality bias impairs collective decision-making across cultures. Proc Natl Acad Sci U S A. 2015; 112(12):3835-40. PMC: 4378431. DOI: 10.1073/pnas.1421692112. View

Mars R, Sallet J, Neubert F, Rushworth M . Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex. Proc Natl Acad Sci U S A. 2013; 110(26):10806-11. PMC: 3696774. DOI: 10.1073/pnas.1302956110. View

Pescetelli N, Yeung N . The role of decision confidence in advice-taking and trust formation. J Exp Psychol Gen. 2020; 150(3):507-526. DOI: 10.1037/xge0000960. View

Behrens T, Hunt L, Woolrich M, Rushworth M . Associative learning of social value. Nature. 2008; 456(7219):245-9. PMC: 2605577. DOI: 10.1038/nature07538. View

Jamali M, Grannan B, Fedorenko E, Saxe R, Baez-Mendoza R, Williams Z . Single-neuronal predictions of others' beliefs in humans. Nature. 2021; 591(7851):610-614. PMC: 7990696. DOI: 10.1038/s41586-021-03184-0. View

Baez-Mendoza R, Mastrobattista E, Wang A, Williams Z . Social agent identity cells in the prefrontal cortex of interacting groups of primates. Science. 2021; 374(6566):eabb4149. PMC: 8571805. DOI: 10.1126/science.abb4149. View

Miller K, Botvinick M, Brody C . Value representations in the rodent orbitofrontal cortex drive learning, not choice. Elife. 2022; 11. PMC: 9462853. DOI: 10.7554/eLife.64575. View

Jenkinson M, Beckmann C, Behrens T, Woolrich M, Smith S . FSL. Neuroimage. 2011; 62(2):782-90. DOI: 10.1016/j.neuroimage.2011.09.015. View

10.

Emery N . The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev. 2000; 24(6):581-604. DOI: 10.1016/s0149-7634(00)00025-7. View

11.

Khalighinejad N, Bongioanni A, Verhagen L, Folloni D, Attali D, Aubry J . A Basal Forebrain-Cingulate Circuit in Macaques Decides It Is Time to Act. Neuron. 2019; 105(2):370-384.e8. PMC: 6975166. DOI: 10.1016/j.neuron.2019.10.030. View

12.

Bertini G, Buffalo E, de Weerd P, Desimone R, Ungerleider L . Visual responses to targets and distracters by inferior temporal neurons after lesions of extrastriate areas V4 and TEO. Neuroreport. 2004; 15(10):1611-5. DOI: 10.1097/01.wnr.0000134847.86625.15. View

13.

Brainard D . The Psychophysics Toolbox. Spat Vis. 1997; 10(4):433-6. View

14.

Rudebeck P, Saunders R, Lundgren D, Murray E . Specialized Representations of Value in the Orbital and Ventrolateral Prefrontal Cortex: Desirability versus Availability of Outcomes. Neuron. 2017; 95(5):1208-1220.e5. PMC: 5600902. DOI: 10.1016/j.neuron.2017.07.042. View

15.

Mansouri F, Koechlin E, Rosa M, Buckley M . Managing competing goals - a key role for the frontopolar cortex. Nat Rev Neurosci. 2017; 18(11):645-657. DOI: 10.1038/nrn.2017.111. View

16.

Ernst M, Banks M . Humans integrate visual and haptic information in a statistically optimal fashion. Nature. 2002; 415(6870):429-33. DOI: 10.1038/415429a. View

17.

Park S, Goiame S, OConnor D, Dreher J . Integration of individual and social information for decision-making in groups of different sizes. PLoS Biol. 2017; 15(6):e2001958. PMC: 5489145. DOI: 10.1371/journal.pbio.2001958. View

18.

Bichot N, Xu R, Ghadooshahy A, Williams M, Desimone R . The role of prefrontal cortex in the control of feature attention in area V4. Nat Commun. 2019; 10(1):5727. PMC: 6915702. DOI: 10.1038/s41467-019-13761-7. View

19.

Freiwald W, Tsao D . Functional compartmentalization and viewpoint generalization within the macaque face-processing system. Science. 2010; 330(6005):845-51. PMC: 3181095. DOI: 10.1126/science.1194908. View

20.

Mahmoodi A, Nili H, Harbison C, Hamilton S, Trudel N, Bang D . Causal role of a neural system for separating and selecting multidimensional social cognitive information. Neuron. 2023; 111(7):1152-1164.e6. PMC: 10914676. DOI: 10.1016/j.neuron.2022.12.030. View