Skip to main content
Erschienen in: Brain Structure and Function 1/2017

03.06.2016 | Original Article

Task modulated brain connectivity of the amygdala: a meta-analysis of psychophysiological interactions

verfasst von: Xin Di, Jia Huang, Bharat B. Biswal

Erschienen in: Brain Structure and Function | Ausgabe 1/2017

Einloggen, um Zugang zu erhalten

Abstract

Understanding functional connectivity of the amygdala with other brain regions, especially task modulated connectivity, is a critical step toward understanding the role of the amygdala in emotional processes and the interactions between emotion and cognition. The present study performed coordinate-based meta-analysis on studies of task modulated connectivity of the amygdala which used psychophysiological interaction (PPI) analysis. We first analyzed 49 PPI studies on different types of tasks using activation likelihood estimation (ALE) meta-analysis. Widespread cortical and subcortical regions showed consistent task modulated connectivity with the amygdala, including the medial frontal cortex, bilateral insula, anterior cingulate, fusiform gyrus, parahippocampal gyrus, thalamus, and basal ganglia. These regions were in general overlapped with those showed coactivations with the amygdala, suggesting that these regions and amygdala are not only activated together, but also show different levels of interactions during tasks. Further analyses with subsets of PPI studies revealed task specific functional connectivities with the amygdala that were modulated by fear processing, face processing, and emotion regulation. These results suggest a dynamic modulation of connectivity upon task demands, and provide new insights on the functions of the amygdala in different affective and cognitive processes. The meta-analytic approach on PPI studies may offer a framework toward systematical examinations of task modulated connectivity.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Adolphs R, Tranel D, Damasio H, Damasio A (1994) Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372:669–672. doi:10.1038/372669a0 CrossRefPubMed Adolphs R, Tranel D, Damasio H, Damasio A (1994) Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372:669–672. doi:10.​1038/​372669a0 CrossRefPubMed
Zurück zum Zitat Blasi G, Lo Bianco L, Taurisano P, Gelao B, Romano R, Fazio L, Papazacharias A, Di Giorgio A, Caforio G, Rampino A, Masellis R, Papp A, Ursini G, Sinibaldi L, Popolizio T, Sadee W, Bertolino A (2009) Functional variation of the dopamine D2 receptor gene is associated with emotional control as well as brain activity and connectivity during emotion processing in humans. J Neurosci 29:14812–14819. doi:10.1523/JNEUROSCI.3609-09.2009 CrossRefPubMedPubMedCentral Blasi G, Lo Bianco L, Taurisano P, Gelao B, Romano R, Fazio L, Papazacharias A, Di Giorgio A, Caforio G, Rampino A, Masellis R, Papp A, Ursini G, Sinibaldi L, Popolizio T, Sadee W, Bertolino A (2009) Functional variation of the dopamine D2 receptor gene is associated with emotional control as well as brain activity and connectivity during emotion processing in humans. J Neurosci 29:14812–14819. doi:10.​1523/​JNEUROSCI.​3609-09.​2009 CrossRefPubMedPubMedCentral
Zurück zum Zitat Chan RCK, Di X, McAlonan GM, Gong Q (2011) Brain anatomical abnormalities in high-risk individuals, first-episode, and chronic schizophrenia: an activation likelihood estimation meta-analysis of illness progression. Schizophr Bull 37:177–188. doi:10.1093/schbul/sbp073 CrossRefPubMed Chan RCK, Di X, McAlonan GM, Gong Q (2011) Brain anatomical abnormalities in high-risk individuals, first-episode, and chronic schizophrenia: an activation likelihood estimation meta-analysis of illness progression. Schizophr Bull 37:177–188. doi:10.​1093/​schbul/​sbp073 CrossRefPubMed
Zurück zum Zitat Cisler JM, Bush K, Steele JS (2013) A comparison of statistical methods for detecting context-modulated functional connectivity in fMRI. Neuroimage Cisler JM, Bush K, Steele JS (2013) A comparison of statistical methods for detecting context-modulated functional connectivity in fMRI. Neuroimage
Zurück zum Zitat Di X, Chan RCK, Gong Q (2009) White matter reduction in patients with schizophrenia as revealed by voxel-based morphometry: an activation likelihood estimation meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 33:1390–1394. doi:10.1016/j.pnpbp.2009.08.020 CrossRefPubMed Di X, Chan RCK, Gong Q (2009) White matter reduction in patients with schizophrenia as revealed by voxel-based morphometry: an activation likelihood estimation meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 33:1390–1394. doi:10.​1016/​j.​pnpbp.​2009.​08.​020 CrossRefPubMed
Zurück zum Zitat Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907–2926. doi:10.1002/hbm.20718 CrossRefPubMedPubMedCentral Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907–2926. doi:10.​1002/​hbm.​20718 CrossRefPubMedPubMedCentral
Zurück zum Zitat Fox PT, Laird AR, Fox SP, Fox PM, Uecker AM, Crank M, Koenig SF, Lancaster JL (2005) BrainMap taxonomy of experimental design: description and evaluation. Hum Brain Mapp 25:185–198. doi:10.1002/hbm.20141 CrossRefPubMed Fox PT, Laird AR, Fox SP, Fox PM, Uecker AM, Crank M, Koenig SF, Lancaster JL (2005) BrainMap taxonomy of experimental design: description and evaluation. Hum Brain Mapp 25:185–198. doi:10.​1002/​hbm.​20141 CrossRefPubMed
Zurück zum Zitat Friedel E, Schlagenhauf F, Sterzer P, Park SQ, Bermpohl F, Ströhle A, Stoy M, Puls I, Hägele C, Wrase J, Büchel C, Heinz A (2009) 5-HTT genotype effect on prefrontal-amygdala coupling differs between major depression and controls. Psychopharmacology 205:261–271. doi:10.1007/s00213-009-1536-1 CrossRefPubMed Friedel E, Schlagenhauf F, Sterzer P, Park SQ, Bermpohl F, Ströhle A, Stoy M, Puls I, Hägele C, Wrase J, Büchel C, Heinz A (2009) 5-HTT genotype effect on prefrontal-amygdala coupling differs between major depression and controls. Psychopharmacology 205:261–271. doi:10.​1007/​s00213-009-1536-1 CrossRefPubMed
Zurück zum Zitat Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6:218–229CrossRefPubMed Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6:218–229CrossRefPubMed
Zurück zum Zitat Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, Benedetti F, Abbamonte M, Gasparotti R, Barale F, Perez J, McGuire P, Politi P (2009) Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 34:418–432PubMedPubMedCentral Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, Benedetti F, Abbamonte M, Gasparotti R, Barale F, Perez J, McGuire P, Politi P (2009) Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 34:418–432PubMedPubMedCentral
Zurück zum Zitat Gitelman DR, Penny WD, Ashburner J, Friston KJ (2003) Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 19:200–207CrossRefPubMed Gitelman DR, Penny WD, Ashburner J, Friston KJ (2003) Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 19:200–207CrossRefPubMed
Zurück zum Zitat Kim J, Horwitz B (2008) Investigating the neural basis for fMRI-based functional connectivity in a blocked design: application to interregional correlations and psycho-physiological interactions. Magn Reson Imaging 26:583–593. doi:10.1016/j.mri.2007.10.011 CrossRefPubMed Kim J, Horwitz B (2008) Investigating the neural basis for fMRI-based functional connectivity in a blocked design: application to interregional correlations and psycho-physiological interactions. Magn Reson Imaging 26:583–593. doi:10.​1016/​j.​mri.​2007.​10.​011 CrossRefPubMed
Zurück zum Zitat Laird AR, Fox PM, Price CJ, Glahn DC, Uecker AM, Lancaster JL, Turkeltaub PE, Kochunov P, Fox PT (2005a) ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp 25:155–164. doi:10.1002/hbm.20136 CrossRefPubMed Laird AR, Fox PM, Price CJ, Glahn DC, Uecker AM, Lancaster JL, Turkeltaub PE, Kochunov P, Fox PT (2005a) ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp 25:155–164. doi:10.​1002/​hbm.​20136 CrossRefPubMed
Zurück zum Zitat Laird AR, Lancaster JL, Fox PT (2005b) BrainMap: the social evolution of a human brain mapping database. Neuroinformatics 3:65–78CrossRefPubMed Laird AR, Lancaster JL, Fox PT (2005b) BrainMap: the social evolution of a human brain mapping database. Neuroinformatics 3:65–78CrossRefPubMed
Zurück zum Zitat Laird AR, Robinson JL, McMillan KM, Tordesillas-Gutiérrez D, Moran ST, Gonzales SM, Ray KL, Franklin C, Glahn DC, Fox PT, Lancaster JL (2010) Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: validation of the Lancaster transform. Neuroimage 51:677–683. doi:10.1016/j.neuroimage.2010.02.048 CrossRefPubMedPubMedCentral Laird AR, Robinson JL, McMillan KM, Tordesillas-Gutiérrez D, Moran ST, Gonzales SM, Ray KL, Franklin C, Glahn DC, Fox PT, Lancaster JL (2010) Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: validation of the Lancaster transform. Neuroimage 51:677–683. doi:10.​1016/​j.​neuroimage.​2010.​02.​048 CrossRefPubMedPubMedCentral
Zurück zum Zitat Lancaster JL, Tordesillas-Gutiérrez D, Martinez M, Salinas F, Evans A, Zilles K, Mazziotta JC, Fox PT (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28:1194–1205. doi:10.1002/hbm.20345 CrossRefPubMed Lancaster JL, Tordesillas-Gutiérrez D, Martinez M, Salinas F, Evans A, Zilles K, Mazziotta JC, Fox PT (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28:1194–1205. doi:10.​1002/​hbm.​20345 CrossRefPubMed
Zurück zum Zitat Lemogne C, Gorwood P, Boni C, Pessiglione M, Lehéricy S, Fossati P (2011) Cognitive appraisal and life stress moderate the effects of the 5-HTTLPR polymorphism on amygdala reactivity. Hum Brain Mapp 32:1856–1867. doi:10.1002/hbm.21150 CrossRefPubMed Lemogne C, Gorwood P, Boni C, Pessiglione M, Lehéricy S, Fossati P (2011) Cognitive appraisal and life stress moderate the effects of the 5-HTTLPR polymorphism on amygdala reactivity. Hum Brain Mapp 32:1856–1867. doi:10.​1002/​hbm.​21150 CrossRefPubMed
Zurück zum Zitat Madsen MK, Mc Mahon B, Andersen SB, Siebner HR, Knudsen GM, Fisher PM (2016) Threat-related amygdala functional connectivity is associated with 5-HTTLPR genotype and neuroticism. Soc Cogn Affect Neurosci 11:140–149. doi:10.1093/scan/nsv098 CrossRefPubMed Madsen MK, Mc Mahon B, Andersen SB, Siebner HR, Knudsen GM, Fisher PM (2016) Threat-related amygdala functional connectivity is associated with 5-HTTLPR genotype and neuroticism. Soc Cogn Affect Neurosci 11:140–149. doi:10.​1093/​scan/​nsv098 CrossRefPubMed
Zurück zum Zitat Phillips ML, Young AW, Senior C, Brammer M, Andrew C, Calder AJ, Bullmore ET, Perrett DI, Rowland D, Williams SC, Gray JA, David AS (1997) A specific neural substrate for perceiving facial expressions of disgust. Nature 389:495–498. doi:10.1038/39051 CrossRefPubMed Phillips ML, Young AW, Senior C, Brammer M, Andrew C, Calder AJ, Bullmore ET, Perrett DI, Rowland D, Williams SC, Gray JA, David AS (1997) A specific neural substrate for perceiving facial expressions of disgust. Nature 389:495–498. doi:10.​1038/​39051 CrossRefPubMed
Zurück zum Zitat Puglia MH, Lillard TS, Morris JP, Connelly JJ (2015) Epigenetic modification of the oxytocin receptor gene influences the perception of anger and fear in the human brain. Proc Natl Acad Sci USA. 1422096112. doi:10.1073/pnas.1422096112 Puglia MH, Lillard TS, Morris JP, Connelly JJ (2015) Epigenetic modification of the oxytocin receptor gene influences the perception of anger and fear in the human brain. Proc Natl Acad Sci USA. 1422096112. doi:10.​1073/​pnas.​1422096112
Zurück zum Zitat Rasch B, Spalek K, Buholzer S, Luechinger R, Boesiger P, Papassotiropoulos A, de Quervain DJ-F (2009) A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proc Natl Acad Sci USA 106:19191–19196. doi:10.1073/pnas.0907425106 CrossRefPubMedPubMedCentral Rasch B, Spalek K, Buholzer S, Luechinger R, Boesiger P, Papassotiropoulos A, de Quervain DJ-F (2009) A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proc Natl Acad Sci USA 106:19191–19196. doi:10.​1073/​pnas.​0907425106 CrossRefPubMedPubMedCentral
Zurück zum Zitat Rasch B, Spalek K, Buholzer S, Luechinger R, Boesiger P, de Quervain DJ-F, Papassotiropoulos A (2010) Aversive stimuli lead to differential amygdala activation and connectivity patterns depending on catechol-O-methyltransferase Val158Met genotype. Neuroimage 52:1712–1719. doi:10.1016/j.neuroimage.2010.05.054 CrossRefPubMed Rasch B, Spalek K, Buholzer S, Luechinger R, Boesiger P, de Quervain DJ-F, Papassotiropoulos A (2010) Aversive stimuli lead to differential amygdala activation and connectivity patterns depending on catechol-O-methyltransferase Val158Met genotype. Neuroimage 52:1712–1719. doi:10.​1016/​j.​neuroimage.​2010.​05.​054 CrossRefPubMed
Zurück zum Zitat Sladky R, Hoflich A, Kublbock M, Kraus C, Baldinger P, Moser E, Lanzenberger R, Windischberger C (2015) Disrupted effective connectivity between the amygdala and orbitofrontal cortex in social anxiety disorder during emotion discrimination revealed by dynamic causal modeling for fMRI. Cereb Cortex 25:895–903. doi:10.1093/cercor/bht279 CrossRefPubMed Sladky R, Hoflich A, Kublbock M, Kraus C, Baldinger P, Moser E, Lanzenberger R, Windischberger C (2015) Disrupted effective connectivity between the amygdala and orbitofrontal cortex in social anxiety disorder during emotion discrimination revealed by dynamic causal modeling for fMRI. Cereb Cortex 25:895–903. doi:10.​1093/​cercor/​bht279 CrossRefPubMed
Zurück zum Zitat Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York
Zurück zum Zitat Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P (2012) Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum Brain Mapp 33:1–13. doi:10.1002/hbm.21186 CrossRefPubMed Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P (2012) Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum Brain Mapp 33:1–13. doi:10.​1002/​hbm.​21186 CrossRefPubMed
Zurück zum Zitat Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418. 9412517 Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418. 9412517
Zurück zum Zitat Wu M, Kujawa A, Lu LH, Fitzgerald DA, Klumpp H, Fitzgerald KD, Monk CS, Phan KL (2016) Age-related changes in amygdala-frontal connectivity during emotional face processing from childhood into young adulthood. Hum Brain Mapp. doi:10.1002/hbm.23129 Wu M, Kujawa A, Lu LH, Fitzgerald DA, Klumpp H, Fitzgerald KD, Monk CS, Phan KL (2016) Age-related changes in amygdala-frontal connectivity during emotional face processing from childhood into young adulthood. Hum Brain Mapp. doi:10.​1002/​hbm.​23129
Zurück zum Zitat Yoder KJ, Porges EC, Decety J (2015) Amygdala subnuclei connectivity in response to violence reveals unique influences of individual differences in psychopathic traits in a nonforensic sample. Hum Brain Mapp 36:1417–1428. doi:10.1002/hbm.22712 CrossRefPubMed Yoder KJ, Porges EC, Decety J (2015) Amygdala subnuclei connectivity in response to violence reveals unique influences of individual differences in psychopathic traits in a nonforensic sample. Hum Brain Mapp 36:1417–1428. doi:10.​1002/​hbm.​22712 CrossRefPubMed
Metadaten
Titel
Task modulated brain connectivity of the amygdala: a meta-analysis of psychophysiological interactions
verfasst von
Xin Di
Jia Huang
Bharat B. Biswal
Publikationsdatum
03.06.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 1/2017
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1239-4

Weitere Artikel der Ausgabe 1/2017

Brain Structure and Function 1/2017 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.