Functional connectivity dynamics during film viewing reveal common networks for different emotional experiences

Gal Raz; Alexandra Touroutoglou; Christine Wilson-Mendenhall; Gadi Gilam; Tamar Lin; Tal Gonen; Yael Jacob; Shir Atzil; Roee Admon; Maya Bleich-Cohen; Adi Maron-Katz; Talma Hendler; Lisa Feldman Barrett

doi:10.3758/s13415-016-0425-4

Functional connectivity dynamics during film viewing reveal common networks for different emotional experiences

Gal Raz, Alexandra Touroutoglou, Christine Wilson-Mendenhall, Gadi Gilam, Tamar Lin, Tal Gonen, Yael Jacob, Shir Atzil, Roee Admon, Maya Bleich-Cohen, Adi Maron-Katz, Talma Hendler, Lisa Feldman Barrett^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

65 Scopus citations

Abstract

Recent theoretical and empirical work has highlighted the role of domain-general, large-scale brain networks in generating emotional experiences. These networks are hypothesized to process aspects of emotional experiences that are not unique to a specific emotional category (e.g., “sadness,” “happiness”), but rather that generalize across categories. In this article, we examined the dynamic interactions (i.e., changing cohesiveness) between specific domain-general networks across time while participants experienced various instances of sadness, fear, and anger. We used a novel method for probing the network connectivity dynamics between two salience networks and three amygdala-based networks. We hypothesized, and found, that the functional connectivity between these networks covaried with the intensity of different emotional experiences. Stronger connectivity between the dorsal salience network and the medial amygdala network was associated with more intense ratings of emotional experience across six different instances of the three emotion categories examined. Also, stronger connectivity between the dorsal salience network and the ventrolateral amygdala network was associated with more intense ratings of emotional experience across five out of the six different instances. Our findings demonstrate that a variety of emotional experiences are associated with dynamic interactions of domain-general neural systems.

Original language	American English
Pages (from-to)	709-723
Number of pages	15
Journal	Cognitive, Affective and Behavioral Neuroscience
Volume	16
Issue number	4
DOIs	https://doi.org/10.3758/s13415-016-0425-4
State	Published - 1 Aug 2016
Externally published	Yes

Bibliographical note

Funding Information:
We thank Alaina Baker for her assistance with editing the manuscript. This work was supported by a National Institutes of Health Director’s Pioneer Award (DP1OD003312) to L.F.B., a National Institute on Aging grant (R01 AG030311-06A1) to L.F.B., and Shared Instrumentation grants (1S10RR023401, 1S10RR019307, and 1S10RR023043) from the National Center for Research Resources. This study was also supported by a Dan David Scholarship to G.R., and by grants from the University of Chicago’s Arete Initiative “The Science of Virtues,” to T.H., G.R., and G.G.; the Israeli Defense Forces Medical Corps, to T.H. and R.A.; the U.S Department of Defense (W81XWH-11-2-0008) to T.H.; and BRAINTRAIN under the EU FP7 Health Cooperation Work Program (602186), to T.H. and G.R. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Research Resources, the National Institutes of Health, or the National Institute on Aging. G.R., A.T., C.W.-M., S.A., T.H., and L.F.B. designed the study. G.R., A.T., T.H., and L.F.B. wrote the manuscript. G.R., A.T., T.H., L.F.B., G.G., C.W.-M., T.L., T.G., Y.J., S.A., R.A., and A.M.-K. analyzed the data. L.F.B. and T.H. contributed to the grant funding. The authors declare no conflicts of interest.

Publisher Copyright:
© 2016, Psychonomic Society, Inc.

Keywords

Amygdala
Emotions
Network cohesion
Stimulus-induced functional connectivity

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10.3758/s13415-016-0425-4

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Raz, G., Touroutoglou, A., Wilson-Mendenhall, C., Gilam, G., Lin, T., Gonen, T., Jacob, Y., Atzil, S., Admon, R., Bleich-Cohen, M., Maron-Katz, A., Hendler, T., & Barrett, L. F. (2016). Functional connectivity dynamics during film viewing reveal common networks for different emotional experiences. Cognitive, Affective and Behavioral Neuroscience, 16(4), 709-723. https://doi.org/10.3758/s13415-016-0425-4

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title = "Functional connectivity dynamics during film viewing reveal common networks for different emotional experiences",

abstract = "Recent theoretical and empirical work has highlighted the role of domain-general, large-scale brain networks in generating emotional experiences. These networks are hypothesized to process aspects of emotional experiences that are not unique to a specific emotional category (e.g., “sadness,” “happiness”), but rather that generalize across categories. In this article, we examined the dynamic interactions (i.e., changing cohesiveness) between specific domain-general networks across time while participants experienced various instances of sadness, fear, and anger. We used a novel method for probing the network connectivity dynamics between two salience networks and three amygdala-based networks. We hypothesized, and found, that the functional connectivity between these networks covaried with the intensity of different emotional experiences. Stronger connectivity between the dorsal salience network and the medial amygdala network was associated with more intense ratings of emotional experience across six different instances of the three emotion categories examined. Also, stronger connectivity between the dorsal salience network and the ventrolateral amygdala network was associated with more intense ratings of emotional experience across five out of the six different instances. Our findings demonstrate that a variety of emotional experiences are associated with dynamic interactions of domain-general neural systems.",

keywords = "Amygdala, Emotions, Network cohesion, Stimulus-induced functional connectivity",

author = "Gal Raz and Alexandra Touroutoglou and Christine Wilson-Mendenhall and Gadi Gilam and Tamar Lin and Tal Gonen and Yael Jacob and Shir Atzil and Roee Admon and Maya Bleich-Cohen and Adi Maron-Katz and Talma Hendler and Barrett, {Lisa Feldman}",

note = "Funding Information: We thank Alaina Baker for her assistance with editing the manuscript. This work was supported by a National Institutes of Health Director{\textquoteright}s Pioneer Award (DP1OD003312) to L.F.B., a National Institute on Aging grant (R01 AG030311-06A1) to L.F.B., and Shared Instrumentation grants (1S10RR023401, 1S10RR019307, and 1S10RR023043) from the National Center for Research Resources. This study was also supported by a Dan David Scholarship to G.R., and by grants from the University of Chicago{\textquoteright}s Arete Initiative “The Science of Virtues,” to T.H., G.R., and G.G.; the Israeli Defense Forces Medical Corps, to T.H. and R.A.; the U.S Department of Defense (W81XWH-11-2-0008) to T.H.; and BRAINTRAIN under the EU FP7 Health Cooperation Work Program (602186), to T.H. and G.R. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Research Resources, the National Institutes of Health, or the National Institute on Aging. G.R., A.T., C.W.-M., S.A., T.H., and L.F.B. designed the study. G.R., A.T., T.H., and L.F.B. wrote the manuscript. G.R., A.T., T.H., L.F.B., G.G., C.W.-M., T.L., T.G., Y.J., S.A., R.A., and A.M.-K. analyzed the data. L.F.B. and T.H. contributed to the grant funding. The authors declare no conflicts of interest. Publisher Copyright: {\textcopyright} 2016, Psychonomic Society, Inc.",

year = "2016",

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doi = "10.3758/s13415-016-0425-4",

language = "American English",

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Raz, G, Touroutoglou, A, Wilson-Mendenhall, C, Gilam, G, Lin, T, Gonen, T, Jacob, Y, Atzil, S, Admon, R, Bleich-Cohen, M, Maron-Katz, A, Hendler, T & Barrett, LF 2016, 'Functional connectivity dynamics during film viewing reveal common networks for different emotional experiences', Cognitive, Affective and Behavioral Neuroscience, vol. 16, no. 4, pp. 709-723. https://doi.org/10.3758/s13415-016-0425-4

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AU - Touroutoglou, Alexandra

AU - Wilson-Mendenhall, Christine

AU - Gilam, Gadi

AU - Lin, Tamar

AU - Gonen, Tal

AU - Jacob, Yael

AU - Atzil, Shir

AU - Admon, Roee

AU - Bleich-Cohen, Maya

AU - Maron-Katz, Adi

AU - Hendler, Talma

AU - Barrett, Lisa Feldman

N1 - Funding Information: We thank Alaina Baker for her assistance with editing the manuscript. This work was supported by a National Institutes of Health Director’s Pioneer Award (DP1OD003312) to L.F.B., a National Institute on Aging grant (R01 AG030311-06A1) to L.F.B., and Shared Instrumentation grants (1S10RR023401, 1S10RR019307, and 1S10RR023043) from the National Center for Research Resources. This study was also supported by a Dan David Scholarship to G.R., and by grants from the University of Chicago’s Arete Initiative “The Science of Virtues,” to T.H., G.R., and G.G.; the Israeli Defense Forces Medical Corps, to T.H. and R.A.; the U.S Department of Defense (W81XWH-11-2-0008) to T.H.; and BRAINTRAIN under the EU FP7 Health Cooperation Work Program (602186), to T.H. and G.R. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Research Resources, the National Institutes of Health, or the National Institute on Aging. G.R., A.T., C.W.-M., S.A., T.H., and L.F.B. designed the study. G.R., A.T., T.H., and L.F.B. wrote the manuscript. G.R., A.T., T.H., L.F.B., G.G., C.W.-M., T.L., T.G., Y.J., S.A., R.A., and A.M.-K. analyzed the data. L.F.B. and T.H. contributed to the grant funding. The authors declare no conflicts of interest. Publisher Copyright: © 2016, Psychonomic Society, Inc.

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N2 - Recent theoretical and empirical work has highlighted the role of domain-general, large-scale brain networks in generating emotional experiences. These networks are hypothesized to process aspects of emotional experiences that are not unique to a specific emotional category (e.g., “sadness,” “happiness”), but rather that generalize across categories. In this article, we examined the dynamic interactions (i.e., changing cohesiveness) between specific domain-general networks across time while participants experienced various instances of sadness, fear, and anger. We used a novel method for probing the network connectivity dynamics between two salience networks and three amygdala-based networks. We hypothesized, and found, that the functional connectivity between these networks covaried with the intensity of different emotional experiences. Stronger connectivity between the dorsal salience network and the medial amygdala network was associated with more intense ratings of emotional experience across six different instances of the three emotion categories examined. Also, stronger connectivity between the dorsal salience network and the ventrolateral amygdala network was associated with more intense ratings of emotional experience across five out of the six different instances. Our findings demonstrate that a variety of emotional experiences are associated with dynamic interactions of domain-general neural systems.

AB - Recent theoretical and empirical work has highlighted the role of domain-general, large-scale brain networks in generating emotional experiences. These networks are hypothesized to process aspects of emotional experiences that are not unique to a specific emotional category (e.g., “sadness,” “happiness”), but rather that generalize across categories. In this article, we examined the dynamic interactions (i.e., changing cohesiveness) between specific domain-general networks across time while participants experienced various instances of sadness, fear, and anger. We used a novel method for probing the network connectivity dynamics between two salience networks and three amygdala-based networks. We hypothesized, and found, that the functional connectivity between these networks covaried with the intensity of different emotional experiences. Stronger connectivity between the dorsal salience network and the medial amygdala network was associated with more intense ratings of emotional experience across six different instances of the three emotion categories examined. Also, stronger connectivity between the dorsal salience network and the ventrolateral amygdala network was associated with more intense ratings of emotional experience across five out of the six different instances. Our findings demonstrate that a variety of emotional experiences are associated with dynamic interactions of domain-general neural systems.

KW - Amygdala

KW - Emotions

KW - Network cohesion

KW - Stimulus-induced functional connectivity

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Functional connectivity dynamics during film viewing reveal common networks for different emotional experiences

Abstract

Bibliographical note

Keywords

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