The Extended Neural Architecture of Human Attachment: An fMRI Coordinate-Based Meta-Analysis of Affiliative Studies

Tiago Bortolini; Maria Clara Laport; Sofia Latgé-Tovar; Ronald Fischer; Roland Zahn; Ricardo de Oliveira-Souza; Jorge Moll

doi:10.1016/j.neubiorev.2024.105584

The Extended Neural Architecture of Human Attachment: An fMRI Coordinate-Based Meta-Analysis of Affiliative Studies

Tiago Bortolini^*, Maria Clara Laport, Sofia Latgé-Tovar, Ronald Fischer, Roland Zahn, Ricardo de Oliveira-Souza, Jorge Moll

^*Corresponding author for this work

D’Or Institute for Research and Education
Universidade Federal do Rio de Janeiro
Victoria University of Wellington
1Department of Hepatology, Imperial College London, London, UK. 2Institute of Liver Studies at King's College School of Medicine at King's College Hospital, London, UK. 3Institute of Human Health and Performance, University College London, London, UK. 4Department of Asthma Allergy and Lung Biology, King's College London, London, UK. 5Division of Critical Care Medicine, University of Alberta, Edmonton, Canada.
7Federal University of Rio de Janeiro, Rio de Janeiro, Brazil.

Research output: Contribution to journal › Review article › peer-review

2 Citations (Scopus)

Abstract

Functional imaging studies and clinical evidence indicate that cortical areas relevant to social cognition are closely integrated with evolutionarily conserved basal forebrain structures and neighboring regions, enabling human attachment and affiliative emotions. The neural circuitry of human affiliation is continually being unraveled as functional magnetic resonance imaging (fMRI) becomes increasingly prevalent, with studies examining human brain responses to various attachment figures. However, previous fMRI meta-analyses on affiliative stimuli have encountered challenges, such as low statistical power and the absence of robustness measures. To address these issues, we conducted an exhaustive coordinate-based meta-analysis of 79 fMRI studies, focusing on personalized affiliative stimuli, including one's infants, family, romantic partners, and friends. We employed complementary coordinate-based analyses (Activation Likelihood Estimation and Signed Differential Mapping) and conducted a robustness analysis of the results. Findings revealed cluster convergence in cortical and subcortical structures related to reward and motivation, salience detection, social bonding, and cognition. Our study thoroughly explores the neural correlates underpinning affiliative responses, effectively overcoming the limitations noted in previous meta-analyses. It provides an extensive view of the neural substrates associated with affiliative stimuli, illuminating the intricate interaction between cortical and subcortical regions. Our findings significantly contribute to understanding the neurobiology of human affiliation, expanding the known human attachment circuitry beyond the traditional basal forebrain regions observed in other mammals to include uniquely human isocortical structures.

Original language	English
Article number	105584
Journal	Neuroscience and Biobehavioral Reviews
Volume	159
Early online date	15 Feb 2024
DOIs	https://doi.org/10.1016/j.neubiorev.2024.105584
Publication status	Published - Apr 2024

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title = "The Extended Neural Architecture of Human Attachment: An fMRI Coordinate-Based Meta-Analysis of Affiliative Studies",

abstract = "Functional imaging studies and clinical evidence indicate that cortical areas relevant to social cognition are closely integrated with evolutionarily conserved basal forebrain structures and neighboring regions, enabling human attachment and affiliative emotions. The neural circuitry of human affiliation is continually being unraveled as functional magnetic resonance imaging (fMRI) becomes increasingly prevalent, with studies examining human brain responses to various attachment figures. However, previous fMRI meta-analyses on affiliative stimuli have encountered challenges, such as low statistical power and the absence of robustness measures. To address these issues, we conducted an exhaustive coordinate-based meta-analysis of 79 fMRI studies, focusing on personalized affiliative stimuli, including one's infants, family, romantic partners, and friends. We employed complementary coordinate-based analyses (Activation Likelihood Estimation and Signed Differential Mapping) and conducted a robustness analysis of the results. Findings revealed cluster convergence in cortical and subcortical structures related to reward and motivation, salience detection, social bonding, and cognition. Our study thoroughly explores the neural correlates underpinning affiliative responses, effectively overcoming the limitations noted in previous meta-analyses. It provides an extensive view of the neural substrates associated with affiliative stimuli, illuminating the intricate interaction between cortical and subcortical regions. Our findings significantly contribute to understanding the neurobiology of human affiliation, expanding the known human attachment circuitry beyond the traditional basal forebrain regions observed in other mammals to include uniquely human isocortical structures.",

author = "Tiago Bortolini and Laport, {Maria Clara} and Sofia Latg{\'e}-Tovar and Ronald Fischer and Roland Zahn and {de Oliveira-Souza}, Ricardo and Jorge Moll",

note = "Funding Information: This work was supported by FAPERJ ( E-26/202.962/2015; E-26/201.941/2020; E-26/200.942/2021; E-26/204.626/2021 ), the National Council of Technological and Scientific Development ( 465346/2014-6; 434517/2018-6; 313141/2018-5 ), IDOR intramural grant and the Pioneer Science Initiative ( www.pioneerscience.org ). The funding sources had no involvement in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication. Publisher Copyright: {\textcopyright} 2024",

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doi = "10.1016/j.neubiorev.2024.105584",

language = "English",

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journal = "Neuroscience and Biobehavioral Reviews",

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T2 - An fMRI Coordinate-Based Meta-Analysis of Affiliative Studies

AU - Bortolini, Tiago

AU - Laport, Maria Clara

AU - Latgé-Tovar, Sofia

AU - Fischer, Ronald

AU - Zahn, Roland

AU - de Oliveira-Souza, Ricardo

AU - Moll, Jorge

N1 - Funding Information: This work was supported by FAPERJ ( E-26/202.962/2015; E-26/201.941/2020; E-26/200.942/2021; E-26/204.626/2021 ), the National Council of Technological and Scientific Development ( 465346/2014-6; 434517/2018-6; 313141/2018-5 ), IDOR intramural grant and the Pioneer Science Initiative ( www.pioneerscience.org ). The funding sources had no involvement in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication. Publisher Copyright: © 2024

PY - 2024/4

Y1 - 2024/4

N2 - Functional imaging studies and clinical evidence indicate that cortical areas relevant to social cognition are closely integrated with evolutionarily conserved basal forebrain structures and neighboring regions, enabling human attachment and affiliative emotions. The neural circuitry of human affiliation is continually being unraveled as functional magnetic resonance imaging (fMRI) becomes increasingly prevalent, with studies examining human brain responses to various attachment figures. However, previous fMRI meta-analyses on affiliative stimuli have encountered challenges, such as low statistical power and the absence of robustness measures. To address these issues, we conducted an exhaustive coordinate-based meta-analysis of 79 fMRI studies, focusing on personalized affiliative stimuli, including one's infants, family, romantic partners, and friends. We employed complementary coordinate-based analyses (Activation Likelihood Estimation and Signed Differential Mapping) and conducted a robustness analysis of the results. Findings revealed cluster convergence in cortical and subcortical structures related to reward and motivation, salience detection, social bonding, and cognition. Our study thoroughly explores the neural correlates underpinning affiliative responses, effectively overcoming the limitations noted in previous meta-analyses. It provides an extensive view of the neural substrates associated with affiliative stimuli, illuminating the intricate interaction between cortical and subcortical regions. Our findings significantly contribute to understanding the neurobiology of human affiliation, expanding the known human attachment circuitry beyond the traditional basal forebrain regions observed in other mammals to include uniquely human isocortical structures.

AB - Functional imaging studies and clinical evidence indicate that cortical areas relevant to social cognition are closely integrated with evolutionarily conserved basal forebrain structures and neighboring regions, enabling human attachment and affiliative emotions. The neural circuitry of human affiliation is continually being unraveled as functional magnetic resonance imaging (fMRI) becomes increasingly prevalent, with studies examining human brain responses to various attachment figures. However, previous fMRI meta-analyses on affiliative stimuli have encountered challenges, such as low statistical power and the absence of robustness measures. To address these issues, we conducted an exhaustive coordinate-based meta-analysis of 79 fMRI studies, focusing on personalized affiliative stimuli, including one's infants, family, romantic partners, and friends. We employed complementary coordinate-based analyses (Activation Likelihood Estimation and Signed Differential Mapping) and conducted a robustness analysis of the results. Findings revealed cluster convergence in cortical and subcortical structures related to reward and motivation, salience detection, social bonding, and cognition. Our study thoroughly explores the neural correlates underpinning affiliative responses, effectively overcoming the limitations noted in previous meta-analyses. It provides an extensive view of the neural substrates associated with affiliative stimuli, illuminating the intricate interaction between cortical and subcortical regions. Our findings significantly contribute to understanding the neurobiology of human affiliation, expanding the known human attachment circuitry beyond the traditional basal forebrain regions observed in other mammals to include uniquely human isocortical structures.

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DO - 10.1016/j.neubiorev.2024.105584

M3 - Review article

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SN - 0149-7634

VL - 159

JO - Neuroscience and Biobehavioral Reviews

JF - Neuroscience and Biobehavioral Reviews

M1 - 105584

ER -

The Extended Neural Architecture of Human Attachment: An fMRI Coordinate-Based Meta-Analysis of Affiliative Studies

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