Advertisement

Experimental Brain Research

, Volume 237, Issue 9, pp 2367–2385 | Cite as

Differential functional patterns of the human posterior cingulate cortex during activation and deactivation: a meta-analytic connectivity model

  • Jessica N. BuslerEmail author
  • Julio A. Yanes
  • Ryan T. Bird
  • Meredith A. Reid
  • Jennifer L. Robinson
Research Article

Abstract

The posterior cingulate cortex (PCC) has been implicated in a host of cognitive and behavioral processes in addition to serving as a central hub in the default mode network (DMN). Moreover, the PCC has been shown to be involved in a range of psychiatric and neurological disorders. However, very little is known about the specific activated/deactivated functional profiles of the PCC. Here, we employed a dual analytic approach using robust quantitative meta-analytical connectivity modeling (MACM) and ultra-high field, high resolution resting state functional magnetic resonance imaging (rs-fMRI) to identify state-specific functional activity patterns of the human PCC. The MACM results provided evidence for regions of convergence for PCC co-activation and co-deactivation (i.e., left medial frontal gyrus, left amygdala, and left anterior cingulate) as well as regions of divergence specific to either PCC activation (i.e., bilateral inferior frontal gyri) or PCC deactivation (i.e., left parahippocampal gyrus). In addition, exploratory MACMs on dorsal and ventral subregions of the PCC revealed differential functional activity patterns such as greater co-activation of the right PCC and left inferior parietal lobule with the dorsal PCC and greater co-activation of right precuneus with the ventral PCC. Resting state connectivity analyses showed widespread connectivity similar to that of the PCC co-activation-based MACM, but also demonstrated additional regions of activity, including bilateral superior parietal regions and right superior temporal regions. These analyses highlight the diverse neurofunctional repertoire of the human PCC, provide additional insight into its dynamic functional activity patterns as it switches between activated and deactivated states, and elucidates the cognitive processes that may be implicated in clinical populations.

Keywords

Brain Neuroimaging Magnetic resonance imaging Activation analysis Attention 

Notes

Acknowledgements

A Collaborative Use Agreement exists between JLR and the BrainMap® Database.

Compliance with ethical standards

Conflict of interest

All authors report having no financial, personal, or organizational conflict of interest with the work outlined in this manuscript.

Human and animal rights

The work outlined in this manuscript does not involve the use of human subjects as defined by the Institutional Review Board and no informed consent was necessary.

Supplementary material

221_2019_5595_MOESM1_ESM.jpg (115 kb)
Supplementary material 1 (JPEG 115 kb)

References

  1. Acikalin MY, Gorgolewski KJ, Poldrack RA (2017) A coordinate-based meta-analysis of overlaps in regional specialization and functional connectivity across subjective value and default mode networks. Front Neurosci 11:1–11.  https://doi.org/10.3389/fnins.2017.00001 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Andrews-Hanna JR (2012) The brain’s default network and its adaptive role in internal mentation. The Neuroscientist 18(3):251–270.  https://doi.org/10.1177/1073858411403316 CrossRefPubMedGoogle Scholar
  3. Ashburner J (2012) SPM: a history. NeuroImage 62:791–800CrossRefGoogle Scholar
  4. Bai F, Watson DR, Yu H, Shi Y, Yuan Y, Zhang Z (2009) Abnormal resting-state functional connectivity of posterior cingulate cortex in amnestic type mild cognitive impairment. Brain Res 1302:167–174.  https://doi.org/10.1016/j.brainres.2009.09.028 CrossRefPubMedGoogle Scholar
  5. Barbey AK, Krueger F, Grafman J (2009) Structured event complexes in the medial prefrontal cortex support counterfactual representations for future planning. Philos Trans R Soc B Biol Sci 364(1521):1291–1300.  https://doi.org/10.1098/rstb.2008.0315 CrossRefGoogle Scholar
  6. Barbey AK, Colom R, Paul EJ, Grafman J (2014) Architecture of fluid intelligence and working memory revealed by lesion mapping. Brain Struct Funct 219(2):485–494.  https://doi.org/10.1007/s00429-013-0512-z CrossRefPubMedGoogle Scholar
  7. Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage 37(1):90–101.  https://doi.org/10.1016/J.NEUROIMAGE.2007.04.042 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann NY Acad Sci 1124:1–38.  https://doi.org/10.1196/annals.1440.011 CrossRefPubMedGoogle Scholar
  9. Buckner RL, Krienen FM, Yeo BTT (2013) Opportunities and limitations of intrinsic functional connectivity MRI. Nat Neurosci 16(7):832–837.  https://doi.org/10.1038/nn.3423 CrossRefPubMedGoogle Scholar
  10. Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cognit Sci 4(6):215–222.  https://doi.org/10.1016/S1364-6613(00)01483-2 CrossRefGoogle Scholar
  11. Bzdok D, Heeger A, Langner R, Laird AR, Fox PT, Palomero-Gallagher N, Eickhoff SB (2015) Subspecialization in the human posterior medial cortex. NeuroImage 106:55–71.  https://doi.org/10.1016/j.neuroimage.2014.11.009 CrossRefPubMedGoogle Scholar
  12. Cahill L (2006) Sex-related influences on the neurobiology of emotionally influenced memory. Ann NY Acad Sci 985(1):163–173.  https://doi.org/10.1111/j.1749-6632.2003.tb07080.x CrossRefGoogle Scholar
  13. Campbell KL, Schacter DL (2017) Ageing and the resting state: is cognition obsolete? Lang Cognit Neurosci 32(6):661–668.  https://doi.org/10.1080/23273798.2016.1227858 CrossRefGoogle Scholar
  14. Cha J, Jo HJ, Gibson WS, Lee JM (2017) Functional organization of the human posterior cingulate cortex, revealed by multiple connectivity-based parcellation methods. Hum Brain Mapp 38(6):2808–2818.  https://doi.org/10.1002/hbm.23570 CrossRefPubMedGoogle Scholar
  15. Cherkassky VL, Kana RK, Keller TA, Just MA (2006) Functional connectivity in a baseline resting-state network in autism. NeuroReport 17(16):1687–1690.  https://doi.org/10.1097/01.wnr.0000239956.45448.4c CrossRefPubMedGoogle Scholar
  16. Cole MW, Bassett DS, Power JD, Braver TS, Petersen SE (2014) Intrinsic and task-evoked network architectures of the human brain. Neuron 83(1):238–251.  https://doi.org/10.1016/J.NEURON.2014.05.014 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Craig AD (2009) How do you feel–now? The anterior insula and human awareness. Nat Rev Neurosci 10(1):59–70.  https://doi.org/10.1038/nrn2555 CrossRefPubMedGoogle Scholar
  18. Crick FC, Koch C (2005) What is the function of the claustrum? Philos Trans R Soc Lond B Biol Sci 360(1458):1271–1279.  https://doi.org/10.1098/rstb.2005.1661 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Eickhoff S, Laird A, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based ALE meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30(9):2907–2926.  https://doi.org/10.1002/hbm.20718.Coordinate-based CrossRefPubMedPubMedCentralGoogle Scholar
  20. Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. NeuroImage 59(3):2349–2361.  https://doi.org/10.1016/j.neuroimage.2011.09.017 CrossRefPubMedGoogle Scholar
  21. Eickhoff SB, Laird AR, Fox PM, Lancaster JL, Fox PT (2016) Implementation errors in the GingerALE software: description and recommendations. Human Brain Mapp 15:8.  https://doi.org/10.1002/hbm.23342 CrossRefGoogle Scholar
  22. Fox PT, Laird AR, Fox SP, Fox PM, Uecker AM, Crank M, Lancaster JL (2005) BrainMap taxonomy of experimental design: description and evaluation. IHuman Brain Mapp 25:185–198.  https://doi.org/10.1002/hbm.20141 CrossRefGoogle Scholar
  23. Frankenstein U, Wennerberg A, Richter W, Bernstein C, Morden D, Rémy F, Mcintyre M (2003) Activation and deactivation in blood oxygenation level dependent functional magnetic resonance imaging. Concepts Magn Reson 16A(1):63–70.  https://doi.org/10.1002/cmr.a.10054 CrossRefGoogle Scholar
  24. Fransson P, Marrelec G (2008) The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: evidence from a partial correlation network analysis. Neuroimage 42:1178–1184.  https://doi.org/10.1016/j.neuroimage.2008.05.059 CrossRefPubMedGoogle Scholar
  25. Gilmore AW, Nelson SM, McDermott KB (2015) A parietal memory network revealed by multiple MRI methods. Trends Cognit Sci 19(9):534–543.  https://doi.org/10.1016/j.tics.2015.07.004 CrossRefGoogle Scholar
  26. Gläscher J, Adolphs R, Gläscher J, Adolphs R, Glascher J, Adolphs R (2003) Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. J Neurosci 23(32):10274–10282.  https://doi.org/10.1523/JNEUROSCI.23-32-10274.2003 CrossRefPubMedGoogle Scholar
  27. Hadland K, Rushworth MF, Gaffan D, Passingham R (2003) The effect of cingulate lesions on social behaviour and emotion. Neuropsychologia 41(8):919–931.  https://doi.org/10.1016/S0028-3932(02)00325-1 CrossRefGoogle Scholar
  28. Hale JR, Brookes MJ, Hall EL, Zumer JM, Stevenson CM, Francis ST, Morris PG (2010) Comparison of functional connectivity in default mode and sensorimotor networks at 3 and 7T. Magn Reson Mater Phys 23:339–349.  https://doi.org/10.1007/s10334-010-0220-0 CrossRefGoogle Scholar
  29. Hardee JE, Thompson JC, Puce A (2008) The left amygdala knows fear: laterality in the amygdala response to fearful eyes. Soc Cognit Affect Neurosci 3(1):47–54.  https://doi.org/10.1093/scan/nsn001 CrossRefGoogle Scholar
  30. Hayes DJ, Huxtable AG (2012) Interpreting deactivations in neuroimaging. Front Psychol 3:27.  https://doi.org/10.3389/fpsyg.2012.00027 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kessler D, Angstadt M, Sripada CS (2017) Reevaluating “cluster failure” in fMRI using nonparametric control of the false discovery rate. Proc Natl Acad Sci 114(17):E3372–E3373.  https://doi.org/10.1073/pnas.1614502114 CrossRefPubMedGoogle Scholar
  32. Kjaer TW, Nowak M, Lou HC (2002) Reflective self-awareness and conscious states: pet evidence for a common midline parietofrontal core. NeuroImage 17(2):1080–1086.  https://doi.org/10.1006/NIMG.2002.1230 CrossRefPubMedGoogle Scholar
  33. Krienen FM, Yeo BTT, Buckner RL (2014) Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture. Philos Trans R Soc B Bio Sci 369(1653):20130526.  https://doi.org/10.1098/rstb.2013.0526 CrossRefGoogle Scholar
  34. Kozlovskiy SA, Nikonova EY, Pyasik MM, Velichkovsky BM (2012) The cingulate cortex and human memory processes. Psychol Russia 5:231Google Scholar
  35. Laird AR, Fox PM, Price CJ, Glahn DC, Uecker AM, Lancaster JL, Fox PT (2005a) ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp 25:155–164.  https://doi.org/10.1002/hbm.20136 CrossRefPubMedGoogle Scholar
  36. Laird AR, Lancaster JL, Fox PT (2005b) BrainMap: the social evolution of a human brain mapping database. Neuroinformatics.  https://doi.org/10.1385/NI:3:1:065 CrossRefPubMedGoogle Scholar
  37. Lancaster JL, Laird AR, Eickhoff SB, Martinez MJ, Fox PM, Fox PT (2012) Automated regional behavioral analysis for human brain imaging. Front Neuroinform 6:23.  https://doi.org/10.3389/fninf.2012.00023 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Leech R, Sharp DJ (2014) The role of the posterior cingulate cortex in cognition and disease. Brain 137(1):12–32.  https://doi.org/10.1093/brain/awt162 CrossRefGoogle Scholar
  39. Leech R, Kamourieh S, Beckmann CF, Sharp DJ (2011) Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. J Neurosci 31(9):3217–3224.  https://doi.org/10.1523/JNEUROSCI.5626-10.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Leech R, Braga R, Sharp DJ (2012) Echoes of the brain within the posterior cingulate. Cortex 32(1):215–222.  https://doi.org/10.1523/JNEUROSCI.3689-11.2012 CrossRefGoogle Scholar
  41. Liang M, Zhou Y, Jiang T, Liu Z, Tian L, Liu H, Hao Y (2006) Widespread functional disconnectivity in schizophrenia with resting-state functional magnetic resonance imaging. NeuroReport 17(2):209–213.  https://doi.org/10.1097/01.wnr.0000198434.06518.b8 CrossRefPubMedGoogle Scholar
  42. Lord AR, Li M, Demenescu LR, van den Meer J, Borchardt V, Krause AL, Walter M (2017) Richness in functional connectivity depends on the neuronal integrity within the posterior cingulate cortex. Front Neurosci 11:184.  https://doi.org/10.3389/fnins.2017.00184 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lou HC, Luber B, Crupain M, Keenan JP, Nowak M, Kjaer TW, Lisanby SH (2004) Parietal cortex and representation of the mental Self. Proc Natl Acad Sci USA 101(17):6827–6832.  https://doi.org/10.1073/pnas.0400049101 CrossRefPubMedGoogle Scholar
  44. Maddock RJ, Garrett AS, Buonocore MH (2001) Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval. Neuroscience 104(3):667–676.  https://doi.org/10.1016/S0306-4522(01)00108-7 CrossRefPubMedGoogle Scholar
  45. Maddock RJ, Garrett AS, Buonocore MH (2003) Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Hum Brain Mapp 18(1):30–41.  https://doi.org/10.1002/hbm.10075 CrossRefPubMedGoogle Scholar
  46. Miller CH, Hamilton JP, Sacchet MD, Gotlib IH (2015) Meta-analysis of functional neuroimaging of major depressive disorder in youth. JAMA Psychiatry 72(10):1045–1053.  https://doi.org/10.1001/jamapsychiatry.2015.1376 CrossRefPubMedGoogle Scholar
  47. Nakao T, Radua J, Rubia K, Mataix-Cols D (2011) Gray matter volume abnormalities in ADHD: voxel-based meta-analysis exploring the effects of age and stimulant medication. Am J Psychiatry 168(11):1154–1163.  https://doi.org/10.1176/appi.ajp.2011.11020281 CrossRefPubMedGoogle Scholar
  48. Nowogrodzki A (2018) The world’s strongest MRI machines are pushing human imaging to ne limits. Nature 563:24–26.  https://doi.org/10.1038/d41586-018-07182-7 CrossRefPubMedGoogle Scholar
  49. Radua J, Philips ML, Russell T, Lawrence N, Marshall N, Kalidindi Sl, David AS (2010) Neural response to specific components of fearful faces in healthy and schizophrenic adults. Neuroimage 49(1):939–946.  https://doi.org/10.1016/j.neuroimage.2009.08.030 CrossRefPubMedGoogle Scholar
  50. Raichle ME, Macleod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci 98(2):676–682CrossRefGoogle Scholar
  51. Robinson JL, Laird AR, Glahn DC, Lovallo WR, Fox PT (2009) Metaanalytic connectivity modeling: delineating the functional connectivity of the human amygdala. Hum Brain Mapp.  https://doi.org/10.1002/hbm.20854 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Robinson JL, Erath SA, Kana RK, El-Sheikh M (2018) Neurophysiological differences in the adolescent brain following a single night of restricted sleep—a 7T fMRI study. Dev Cognit Neurosci 31:1–10.  https://doi.org/10.1016/J.DCN.2018.03.012 CrossRefGoogle Scholar
  53. Sämann PG, Wehrle R, Hoehn D, Spoormaker VI, Peters H, Tully C, Czisch M (2011) Development of the brain’s default mode network from wakefulness to slow wave sleep. Cereb Cortex 21(9):2082–2093.  https://doi.org/10.1093/cercor/bhq295 CrossRefPubMedGoogle Scholar
  54. Singh KD, Fawcett IP (2008) Transient and linearly graded deactivation of the human default-mode network by a visual detection task. NeuroImage 41(1):100–112.  https://doi.org/10.1016/j.neuroimage.2008.01.051 CrossRefPubMedGoogle Scholar
  55. Talati A, Hirsch J (2005) Functional specialization within the medial frontal gyrus for perceptual go/no-go decisions based on related information: an fMRI study. J Cognit Neurosci 17(7):981–993.  https://doi.org/10.1162/0898929054475226 CrossRefGoogle Scholar
  56. Tavor I, Parker Jones O, Mars RB, Smith SM, Behrens TE, Jbabdi S (2016) Task-free MRI predicts individual differences in brain activity during task performance. Science 352(6282):216–220.  https://doi.org/10.1126/science.aad8127 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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):1–13.  https://doi.org/10.1002/hbm.21186 CrossRefPubMedGoogle Scholar
  58. van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31(44):15775–15786.  https://doi.org/10.1523/JNEUROSCI.3539-11.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Vogt BA (2016) Midcingulate cortex: structure, connections, homologies, functions and diseases. J Chem Neuroanat 74:28–46.  https://doi.org/10.1016/j.jchemneu.2016.01.010 CrossRefGoogle Scholar
  60. Vogt BA, Laureys S (2005) Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. Prog Brain Res 150:205–217.  https://doi.org/10.1016/S0079-6123(05)50015-3 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Vogt BA, Vogt L, Laureys S (2006) Cytology and functionally correlated circuits of human posterior cingulate areas. Neuroimage 29:452–466.  https://doi.org/10.1016/j.neuroimage.2005.07.048 CrossRefPubMedGoogle Scholar
  62. Vytal K, Hamann S (2010) Neuroimaging support for discrete neural correlates of basic emotions: a voxel-based meta-analysis. Journal of Cogniti Neurosci 22(12):2864–2885.  https://doi.org/10.1162/jocn.2009.21366 CrossRefGoogle Scholar
  63. Whitfield-Gabrieli S, Nieto-Castanon A (2012) Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2:125–141CrossRefGoogle Scholar
  64. Yu C, Zhou Y, Liu Y, Jiang T, Dong H, Zhang Y, Walter M (2011) NeuroImage functional segregation of the human cingulate cortex is con firmed by functional connectivity based neuroanatomical parcellation. NeuroImage 54(4):2571–2581.  https://doi.org/10.1016/j.neuroimage.2010.11.018 CrossRefPubMedGoogle Scholar
  65. Zhu X, Wang X, Xiao J, Liao J, Zhong M, Wang W, Yao S (2012) Evidence of a dissociation pattern in resting-state default mode network connectivity in first-episode, treatment-naive major depression patients. Biol Psychiat 71(7):611–617.  https://doi.org/10.1016/j.biopsych.2011.10.035 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of PsychologyAuburn UniversityAuburnUSA
  2. 2.Auburn University Magnetic Resonance Imaging Research CenterAuburnUSA
  3. 3.Alabama Advanced Imaging ConsortiumAuburn UniversityAuburnUSA
  4. 4.Center for Neuroscience InitiativeAuburn UniversityAuburnUSA

Personalised recommendations