Toward a cumulative science of functional integration: a meta-analysis of psychophysiological interactions
Open accessAbstract
Much of the work in cognitive neuroscience is shifting from a focus on single brain regions to a focus on the connectivity between multiple brain regions. These inter-regional connectivity patterns contribute to a wide range of behaviors and are studied with models of functional integration. The rapid expansion of the literature on functional integration offers an opportunity to scrutinize the consistency and specificity of one of the most popular approaches for quantifying connectivity: psychophysiological interaction (PPI) analysis. We performed coordinate-based meta-analyses on 284 PPI studies, which allowed us to test (a) whether those studies consistently converge on similar target regions and (b) whether the identified target regions are specific to the chosen seed region and psychological context. Our analyses revealed two key results. First, we found that different types of PPI studies-e.g., those using seeds such as amygdala and dorsolateral prefrontal cortex (DLPFC) and contexts such as emotion and cognitive control, respectively-each consistently converge on similar target regions, thus supporting the reliability of PPI as a tool for studying functional integration. Second, we also found target regions that were specific to the chosen seed region and psychological context, indicating distinct patterns of brain connectivity. For example, the DLPFC seed reliably contributed to a posterior cingulate cortex target during cognitive control but contributed to an amygdala target in other contexts. Our results point to the robustness of PPI while highlighting common and distinct patterns of functional integration, potentially advancing models of brain connectivity. Hum Brain Mapp 37:2904-2917, 2016. © 2016 Wiley Periodicals, Inc.
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These results fit with previous work showing a unique functional coupling of DLPFC and PCC in instances of cognitive control.
“These results fit with previous work showing a unique functional coupling of DLPFC and PCC in instances of cognitive control (Smith et al., 2016)”
From Changes in functional connectivity following treatment with emotion regulation therapy (2019) · cites this paper as Smith et al., 2016
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Smith, D. V., Clithero, J. A., Rorden, C., & Karnath, H. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210126110 · Cited by 107 · see citing works
Distributed processing; distributed functions?
Fox, P. T., & Friston, K. J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.051 · Cited by 99 · see citing works
Spatial Attention Evokes Similar Activation Patterns for Visual and Auditory Stimuli
Smith, D. V., Davis, B., Niu, K., Healy, E. W., Bonilha, L., Fridriksson, J., Morgan, P. S., & Rorden, C. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21241 · Cited by 86 · see citing works
The Lateral Occipital Complex Subserves the Perceptual Persistence of Motion-defined Groupings
Ferber, S. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.7.716 · Cited by 84 · see citing works
Meta-analytic connectivity and behavioral parcellation of the human cerebellum
Riedel, M. C., Ray, K. L., Dick, A. S., Sutherland, M. T., Hernandez, Z., Fox, P. M., Eickhoff, S. B., Fox, P. T., & Laird, A. R. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.05.008 · Cited by 69 · see citing works
The effects of attention on the temporal integration of multisensory stimuli
Donohue, S. E., Green, J. J., & Woldorff, M. G. (2015) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2015.00032 · Cited by 59 · see citing works
Cognitive Control Signals in Posterior Cingulate Cortex
Hayden, B. Y., Smith, D. V., & Platt, M. L. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00223 · Cited by 58 · see citing works
Donohue, S. E., Roberts, K., Grent-‘t-Jong, T., & Woldorff, M. G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5298-10.2011 · Cited by 54 · see citing works
Test-retest reliability of dynamic causal modeling for fMRI
Frässle, S., Stephan, K. E., Friston, K. J., Steup, M., Krach, S., Paulus, F. M., & Jansen, A. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.05.040 · Cited by 48 · see citing works
Distinct Reward Properties are Encoded via Corticostriatal Interactions
Smith, D. V., Rigney, A. E., & Delgado, M. R. (2016) · Scientific Reports · doi:10.1038/srep20093 · Cited by 31 · see citing works
Smith, D. V., Sip, K. E., & Delgado, M. R. (2015) · Human Brain Mapping · doi:10.1002/hbm.22804 · Cited by 29 · see citing works
TBSS and probabilistic tractography reveal white matter connections for attention to object features
Mayer, K. M., & Vuong, Q. C. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0631-6 · Cited by 17 · see citing works
Laing, M., Rees, A., & Vuong, Q. C. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01440 · Cited by 8 · see citing works
Fink, G. R., Marshall, J. C., Noth, J., & Zilles, K. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00615-3 · Cited by 4 · see citing works
Flagged first, then by citations
1 of the 111 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Ng, T. H., Alloy, L. B., & Smith, D. V. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0644-x · Cited by 244 · see citing works
Computing the Social Brain Connectome Across Systems and States
Alcalá-López, D., Smallwood, J., Jefferies, E., Overwalle, F. V., Vogeley, K. T., Mars, R. B., Turetsky, B. I., Laird, A. R., Fox, P. T., Eickhoff, S. B., et al. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx121 · Cited by 177 · see citing works
Diano, M., Tamietto, M., Celeghin, A., Weiskrantz, L., Tatu, K., Bagnis, A., Duca, S., Geminiani, G. C., Cauda, F., & Costa, T. (2017) · Scientific Reports · doi:10.1038/srep45260 · Cited by 147 · see citing works
The developing amygdala: a student of the world and a teacher of the cortex
Tottenham, N., & Gabard-Durnam, L. J. (2017) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2017.06.012 · Cited by 130 · see citing works
Di, X., & Biswal, B. B. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy055 · Cited by 106 · see citing works
Multimodal mapping of the face connectome
Wang, Y., Metoki, A., Smith, D. V., Medaglia, J. D., Zang, Y., Benear, S. L., Popal, H. S., Lin, Y., & Olson, I. R. (2020) · Nature Human Behaviour · doi:10.1038/s41562-019-0811-3 · Cited by 88 · see citing works
Functional parcellation of the default mode network: a large-scale meta-analysis
Wang, S., Tepfer, L. J., Taren, A. A., & Smith, D. V. (2020) · Scientific Reports · doi:10.1038/s41598-020-72317-8 · Cited by 79 · see citing works
Yuan, K., Yu, D., Bi, Y., Wang, R., Li, M., Zhang, Y., Dong, M., Zhai, J., Li, Y., Lu, X., et al. (2017) · Human Brain Mapping · doi:10.1002/hbm.23690 · Cited by 75 · see citing works
The neural basis of motivational influences on cognitive control
Parro, C., Dixon, M. L., & Kalina Christoff, A. (2018) · Human Brain Mapping · doi:10.1002/hbm.24348 · Cited by 72 · see citing works
Brain responses to drug cues predict craving changes in abstinent heroin users: A preliminary study
Liu, S., Wang, S., Zhang, M., Xu, Y., Shao, Z., Chen, L., Yang, W., Liu, J., & Yuan, K. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118169 · Cited by 71 · see citing works
Metoki, A., Wang, Y., & Olson, I. R. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab260 · Cited by 70 · see citing works
Changes in functional connectivity following treatment with emotion regulation therapy
Scult, M. A., Fresco, D. M., Gunning, F. M., Liston, C., Seeley, S. H., García, E., & Mennin, D. S. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00010 · Cited by 57 · see citing works
Maliske, L., Schurz, M., & Kanske, P. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105080 · Cited by 61 · see citing works
The neural computation of inconsistent choice behavior
Kurtz-David, V., Persitz, D., Webb, R., & Levy, D. J. (2019) · Nature Communications · doi:10.1038/s41467-019-09343-2 · Cited by 50 · see citing works
Yang, M., Tsai, S. J., & Li, C.-S. R. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-02007-3 · Cited by 55 · see citing works
Age-Dependent Contribution of Domain-General Networks to Semantic Cognition
Martin, S., Saur, D., & Hartwigsen, G. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab252 · Cited by 43 · see citing works
Blunted reward prediction error signals in internet gaming disorder
Lei, W., Liu, K., Chen, G., Tolomeo, S., Liu, C., Peng, Z., Liu, B., Liang, X., Huang, C., Xiang, B., et al. (2020) · Psychological Medicine · doi:10.1017/s003329172000402x · Cited by 43 · see citing works
A large-scale structural and functional connectome of social mentalizing
Wang, Y., Metoki, A., Xia, Y., Zang, Y., He, Y., & Olson, I. R. (2020) · bioRxiv · doi:10.1016/j.neuroimage.2021.118115 · Cited by 34 · see citing works
Connectivity analyses for task-based fMRI
Huang, S., Brigard, F. D., Cabeza, R. E. L., & Davis, S. W. (2024) · Physics of Life Reviews · doi:10.1016/j.plrev.2024.04.012 · Cited by 45 · see citing works
The behavioral and neural basis of empathic blame
Patil, I., Calo, M., fFornasier, F., Cushman, F. A., & Silani, G. (2017) · Scientific Reports · doi:10.1038/s41598-017-05299-9 · Cited by 45 · see citing works
Jiang, K., Yang, Y., Li, L., Li, H., Shen, H., Zhao, F., Xu, Y., & Zheng, A. (2019) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2019.07.003 · Cited by 43 · see citing works
Comparison of whole-brain task-modulated functional connectivity methods for fMRI task connectomics
Masharipov, R. S., Knyazeva, I., Korotkov, A. D., Cherednichenko, D. V., & Kireev, M. V. (2024) · Communications Biology · doi:10.1038/s42003-024-07088-3 · Cited by 38 · see citing works
Zhao, J. L., Liu, J., Jiang, X., Zhou, G., Chen, G., Ding, X. P., Fu, G., & Lee, K. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00452 · Cited by 35 · see citing works
Fareri, D. S., Smith, D. V., & Delgado, M. R. (2020) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsaa031 · Cited by 35 · see citing works
Tusche, A., & Bas, L. M. (2021) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1571 · Cited by 36 · see citing works
Gao, C., Weber, C. E., & Shinkareva, S. V. (2019) · Cortex · doi:10.1016/j.cortex.2019.05.016 · Cited by 35 · see citing works
Fareri, D. S., Hackett, K., Tepfer, L. J., Kelly, V., Henninger, N. M., Reeck, C., Giovannetti, T., & Smith, D. V. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119267 · Cited by 32 · see citing works
Reward enhances connectivity between the ventral striatum and the default mode network
Dobryakova, E., & Smith, D. V. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119398 · Cited by 29 · see citing works
O’Shea, I. M., Popal, H. S., Olson, I. R., Murty, V. P., & Smith, D. V. (2022) · Scientific Reports · doi:10.1038/s41598-022-07020-x · Cited by 27 · see citing works
Disrupted network interactions serve as a neural marker of dyslexia
Turker, S., Kuhnke, P., Jiang, Z., & Hartwigsen, G. (2023) · Communications Biology · doi:10.1038/s42003-023-05499-2 · Cited by 29 · see citing works
How hypnotic suggestions work – A systematic review of prominent theories of hypnosis
Zahedi, A., Lynn, S. J., & Sommer, W. (2024) · Consciousness and Cognition · doi:10.1016/j.concog.2024.103730 · Cited by 34 · see citing works
Sung, D., Park, B., Kim, S.-Y., Kim, B.-N., Park, S., Jung, K.-I., Kim, J., & Park, M.-H. (2020) · Scientific Reports · doi:10.1038/s41598-020-60692-1 · Cited by 24 · see citing works
Reward Sensitivity Enhances Ventrolateral Prefrontal Cortex Activation during Free Choice
Cho, C., Smith, D. V., & Delgado, M. R. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00529 · Cited by 22 · see citing works
Recollection-related increases in functional connectivity across the healthy adult lifespan
King, D. R., de Chastelaine, M., & Rugg, M. D. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.09.026 · Cited by 17 · see citing works
Wyngaarden, J. B., Johnston, C. R., Sazhin, D., Dennison, J. B., Zaff, O., Fareri, D. S., McCloskey, M., Alloy, L. B., Smith, D. V., & Jarcho, J. M. (2024) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsae033 · Cited by 20 · see citing works
Facing temptation: The neural correlates of gambling availability during sports picture exposure
Brevers, D., Herremans, S. C., He, Q., Vanderhasselt, M., Petieau, M., Verdonck, D., Poppa, T., Witte, S. D., Kornreich, C., Bechara, A., et al. (2018) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-018-0599-z · Cited by 19 · see citing works
Smith, D. V., & Delgado, M. R. (2016) · Human Brain Mapping · doi:10.1002/hbm.23354 · Cited by 19 · see citing works
Large-Scale Network Coupling with the Fusiform Cortex Facilitates Future Social Motivation
Utevsky, A. V., Smith, D. V., Young, J. S., & Huettel, S. A. (2017) · eNeuro · doi:10.1523/eneuro.0084-17.2017 · Cited by 19 · see citing works
Diehl, M. M., Lempert, K. M., Parr, A. C., Ballard, I. C., Steele, V. R., & Smith, D. V. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14083 · Cited by 16 · see citing works
Amygdala fMRI—A Critical Appraisal of the Extant Literature
Varkevisser, T., Geuze, E., & van Honk, J. (2024) · Neuroscience Insights · doi:10.1177/26331055241270591 · Cited by 17 · see citing works
The Role of Social Reward and Corticostriatal Connectivity in Substance Use
Sazhin, D., Frazier, A. M., Haynes, C. R., Johnston, C. R., Chat, I. K.-Y., Dennison, J. B., Bart, C. P., McCloskey, M., Chein, J. M., Fareri, D. S., et al. (2020) · Journal of Psychiatry and Brain Science · doi:10.20900/jpbs.20200024 · Cited by 14 · see citing works
Pongpipat, E. E., Kennedy, K. M., Foster, C. M., Boylan, M. A., & Rodrigue, K. M. (2020) · Brain Connectivity · doi:10.1089/brain.2020.0791 · Cited by 12 · see citing works
Wei, X., Chen, J., Zhu, J., Li, Q., Li, W., & Wang, W. (2021) · Brain Imaging and Behavior · doi:10.1007/s11682-020-00447-8 · Cited by 12 · see citing works
A Brief Anatomical Sketch of Human Ventromedial Prefrontal CortexPreprint
Bhanji, J. P., Smith, D. V., & Delgado, M. R. (2019) · doi:10.31234/osf.io/zdt7f · Cited by 12 · see citing works
Huang, Y., Dupont, P. J., de Vliet, L. V., Jastorff, J., Peeters, R. R., Theys, T., Loon, J. V., Paesschen, W. V., den Stock, J. V., & Vandenbulcke, M. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14849 · Cited by 11 · see citing works
Sazhin, D., Wyngaarden, J. Β., Dennison, J. B., Zaff, O., Fareri, D. S., McCloskey, M. S., Alloy, L. B., Jarcho, J. M., & Smith, D. V. (2023) · Biological Psychology · doi:10.1016/j.biopsycho.2024.108857 · Cited by 9 · see citing works
Ventrolateral Prefrontal Cortex Updates Chosen Value According to Choice Set Size
Fujiwara, J., Usui, N., Eifuku, S., Iijima, T., Taira, M., Tsutsui, K., & Tobler, P. N. (2017) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01207 · Cited by 6 · see citing works
Grant Report on Social Reward Learning in Schizophrenia
Butler, P. D., Hoptman, M. J., Smith, D. V., Ermel, J. A., Calderone, D., Lee, S. H., & Barch, D. M. (2020) · Journal of Psychiatry and Brain Science · doi:10.20900/jpbs.20200004 · Cited by 6 · see citing works
Internal reliability of blame-related functional MRI measures in major depressive disorder
Fennema, D., O’Daly, O., Barker, G. J., Moll, J., & Zahn, R. (2021) · NeuroImage Clinical · doi:10.1016/j.nicl.2021.102901 · Cited by 4 · see citing works
Perspectives on the Feldenkrais Method
Russell, R. (2020) · Kinesiology Review · doi:10.1123/kr.2020-0028 · Cited by 4 · see citing works
Age-dependent contribution of domain-general networks to semantic cognitionPreprint
Martin, S., Saur, D., & Hartwigsen, G. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.06.371153 · Cited by 4 · see citing works
Yeung, A. W. K., & Wong, N. S. M. (2025) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2025.1580808 · Cited by 3 · see citing works
Grant Report on the Effects of Childhood Maltreatment on Neurocircuitry in Adolescent Depression
Gillespie, M. L., & Rao, U. (2020) · Journal of Psychiatry and Brain Science · doi:10.20900/jpbs.20200016 · Cited by 3 · see citing works
Wyngaarden, J. Β., Nambiar, A., Dennison, J. B., Alloy, L. B., Fareri, D. S., Jarcho, J. M., & Smith, D. V. (2026) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-025-01396-9 · Cited by 2 · see citing works
Smith, D. V., Zaff, O., Wyngaarden, J. Β., Dennison, J. B., Sazhin, D., Chein, J. M., McCloskey, M., Alloy, L. B., Jarcho, J. M., & Fareri, D. S. (2026) · Biological Psychology · doi:10.1016/j.biopsycho.2026.109209 · Cited by 3 · see citing works
Thalamocortical neural responses during hyperthermia: a resting-state functional MRI study
Zhang, J., Qian, S., Jiang, Q., Gong, G., Liu, K., Li, B., Yin, Y. M., & Sun, G. (2017) · International Journal of Hyperthermia · doi:10.1080/02656736.2017.1382014 · Cited by 1 · see citing works
Divergent Cerebello‐Cortical Network Responses to Emotional Stress in Myoclonus Dystonia
Tarrano, C., Galléa, C., Gomes, M., Brochard, V. B., Anheim, M., Tranchant, C., Thobois, S., Grabli, D., Burbaud, P., Gayraud, D., et al. (2026) · Movement Disorders · doi:10.1002/mds.70159 · Cited by 1 · see citing works
Girard, C., Longo, L., Chesnokova, H., Epinat‐Duclos, J., & Prado, J. (2026) · npj Science of Learning · doi:10.1038/s41539-026-00419-5 · Cited by 1 · see citing works
Diehl, M. M., Lempert, K. M., Parr, A. C., Ballard, I. C., Steele, V. R., & Smith, D. V. (2018) · doi:10.31234/osf.io/yvds9 · Cited by 2 · see citing works
Fareri, D. S., Yang, Y., Ludwig, R. M., Wyngaarden, J. B., Dwamena, D., Hackett, K., Giovannetti, T., & Smith, D. V. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.13.670194
α -tACS Modulates Reward-Dependent Pupil Responses and Corticostriatal ConnectivityPreprint
Smith, D. V., Wyngaarden, J. Β., Weinstein, S. M., Illenberger, N., Liu, Y., Siegel, J., & Krekelberg, B. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.30.702963
- Authors
- Smith, D. V., Gseir, M., Speer, M. E., & Delgado, M. R.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Venue
- Human Brain Mapping
- Publisher
- Wiley
- Published
- 2016-05-04
- Volume
- 37
- Issue
- 8
- Pages
- 2904-2917
- ISSN
- 1065-9471 (ISSN-L)
- 1097-0193
- PMC
- PMC4945436
- OpenAlex
- W2346103131
- Cited by
- 61
- References
- 111
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 5 · 2023: 3 · 2022: 3 · 2021: 7 · 2020: 12 · 2019: 7 · 2018: 5 · 2017: 9 · 2016: 3
- FWCI
- 0.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Human Brain Mapping (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes Health (R01-DA027764, F32-MH107175)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- psychophysiological interaction, functional integration, brain connectivity, amygdala, dorsolateral prefrontal cortex, posterior cingulate cortex, cognitive control, emotions
- MeSH terms
- Brain, Humans, Neural Pathways, Psychophysiology
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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