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A preliminary study on the effects of acute ethanol ingestion on default mode network and temporal fractal properties of the brain

Abstract

Object

To study the effect of acute alcohol intoxication on the functional connectivity of the default mode network (DMN) and temporal fractal properties of the healthy adult brain.

Materials and methods

Eleven healthy male volunteers were asked to drink 0.59 g/kg of ethanol. Resting state blood oxygen level dependent (rsBOLD) MRI scans were obtained before consumption, 60 min post-consumption and 90 min post-consumption. Before each rsBOLD scan, pointed-resolved spectroscopy (PRESS) 1H-MRS (magnetic resonance spectroscopy) scans were acquired to measure ethanol levels in the right basal ganglia.

Results

Significant changes in DMN connectivity were found following alcohol consumption (p < 0.01). Both increased and decreased regional connectivity were found after 60 min, whereas mostly decreased connectivity was found after 90 min. The fractal behaviour of the rsBOLD signal, which is believed to help reveal complexity of small-scale neuronal circuitry, became more ordered after both 60 and 90 min of alcohol consumption (p < 0.01).

Conclusion

The DMN has been linked to personal identity and social behavior. As such, our preliminary findings may provide insight into the neuro-functional underpinnings of the cognitive and behavioral changes observed during acute alcohol intoxication. The reduced fractal dimension implies a change in function of small-scale neural networks towards less complex signaling.

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References

  1. 1.

    Lieberman JA, Tasman A (2006) Handbook of psychiatric drugs, 1st edn. Wiley, Chichester

    Book  Google Scholar 

  2. 2.

    Levin JM, Ross MH, Mendelson JH, Kaufman MJ, Lange N, Maas LC (1998) Reduction in BOLD fMRI response to primary visual stimulation following alcohol ingestion. Psychiatry Res 82(3):135–146

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Calhoun VD, Altschul D, McGinty V, Shih R, Scott D, Sears E (2004) Alcohol intoxication effects on visual perception: an fMRI study. Hum Brain Mapp 21(1):15–26

    PubMed  Article  Google Scholar 

  4. 4.

    Seifritz E, Bilecen D, Hanggi D, Haselhorst R, Radu EW, Wetzel S (2000) Effect of ethanol on BOLD response to acoustic stimulation: implications for neuropharmacological fMRI. Psychiatry Res 99(1):1–13

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Calhoun VD, Pekar JJ, Pearlson GD (2004) Alcohol intoxication effects on simulated driving: exploring alcohol-dose effects on brain activation using functional MRI. Neuropsychopharmacology 29(11):2017–2097

    Article  Google Scholar 

  6. 6.

    Meda SA, Calhoun VD, Astur RS, Turner BM, Ruopp K, Pearlson GD (2009) Alcohol dose effects on brain circuits during simulated driving: an fMRI study. Hum Brain Mapp 30(4):1257–1270

    PubMed Central  PubMed  Article  Google Scholar 

  7. 7.

    Rzepecki-Smith CI, Meda SA, Calhoun VD, Stevens MC, Jafri MJ, Astur RS (2010) Disruptions in functional network connectivity during alcohol intoxicated driving. Alcohol Clin Exp Res 34(3):479–487

    PubMed Central  PubMed  Article  Google Scholar 

  8. 8.

    Van Horn JD, Yanos M, Schmitt PJ, Grafton ST (2006) Alcohol-induced suppression of BOLD activity during goal-directed visuomotor performance. Neuroimage 31(3):1209–1221

    PubMed  Article  Google Scholar 

  9. 9.

    Luchtmann M, Jachau K, Tempelmann C, Bernarding J (2010) Alcohol induced region-dependent alterations of hemodynamic response: implications for the statistical interpretation of pharmacological fMRI studies. Exp Brain Res 204(1):1–10

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  10. 10.

    Paulus MP, Tapert SF, Pulido C, Schuckit MA (2006) Alcohol attenuates load-related activation during a working memory task: relation to level of response to alcohol. Alcohol Clin Exp Res 30(8):1363–1371

    PubMed Central  PubMed  Article  Google Scholar 

  11. 11.

    Trim RS, Simmons AN, Tolentino NJ, Hall SA, Matthews SC, Robinson SK (2010) Acute ethanol effects on brain activation in low- and high-level responders to alcohol. Alcohol Clin Exp Res 34(7):1162–1170

    CAS  PubMed Central  PubMed  Google Scholar 

  12. 12.

    Anderson BM, Stevens MC, Meda SA, Jordan K, Calhoun VD, Pearlson GD (2011) Functional imaging of cognitive control during acute alcohol intoxication. Alcohol Clin Exp Res 35(1):156–165

    PubMed Central  PubMed  Article  Google Scholar 

  13. 13.

    Khalili-Mahani N, Zoethout RM, Beckmann CF, Baerends E, de Kam ML, Soeter RP (2012) Effects of morphine and alcohol on functional brain connectivity during “resting state”: a placebo-controlled crossover study in healthy young men. Hum Brain Mapp 33(5):1003–1018

    PubMed  Article  Google Scholar 

  14. 14.

    Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4):537–541

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103(37):13848–13853

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  16. 16.

    Friston KJ, Frith CD, Liddle PF, Frackowiak RS (1993) Functional connectivity: the principal-component analysis of large (PET) data sets. J Cereb Blood Flow Metab 13(1):5–14

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Esposito F, Pignataro G, Di Renzo G, Spinali A, Paccone A, Tedeschi G (2010) Alcohol increases spontaneous BOLD signal fluctuations in the visual network. Neuroimage 53(2):534–543

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Zarahn E, Aguirre GK, D’Esposito M (1997) Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. Neuroimage 5(3):179–197

    CAS  PubMed  Article  Google Scholar 

  19. 19.

    Mandelbrot B (1967) How long is the coast of Britain? Statistical self-similarity and fractional dimension. Science 156(3775):636–638

    CAS  PubMed  Article  Google Scholar 

  20. 20.

    Maxim V, Sendur L, Fadili J, Suckling J, Gould R, Howard R (2005) Fractional Gaussian noise, functional MRI and Alzheimer’s disease. Neuroimage 25(1):141–158

    PubMed  Article  Google Scholar 

  21. 21.

    Wink AM, Bullmore E, Barnes A, Bernard F, Suckling J (2008) Monofractal and multifractal dynamics of low frequency endogenous brain oscillations in functional MRI. Hum Brain Mapp 29(7):791–801

    PubMed  Article  Google Scholar 

  22. 22.

    Wink AM, Bernard F, Salvador R, Bullmore E, Suckling J (2006) Age and cholinergic effects on hemodynamics and functional coherence of human hippocampus. Neurobiol Aging 27(10):1395–1404

    CAS  PubMed  Article  Google Scholar 

  23. 23.

    Warsi MA, Molloy W, Noseworthy MD (2012) Correlating brain blood oxygenation level dependent (BOLD) fractal dimension mapping with magnetic resonance spectroscopy (MRS) in Alzheimer’s disease. MAGMA 25(5):335–344

    CAS  PubMed  Article  Google Scholar 

  24. 24.

    Lai MC, Lombardo MV, Chakrabarti B, Sadek SA, Pasco G, Wheelwright SJ (2010) A shift to randomness of brain oscillations in people with autism. Biol Psychiatry 68(12):1092–1099

    PubMed  Article  Google Scholar 

  25. 25.

    Jones AW (2010) Evidence-based survey of the elimination rates of ethanol from blood with applications in forensic casework. Forensic Sci Int 200(1–3):1–20

    CAS  PubMed  Article  Google Scholar 

  26. 26.

    Chiu TM, Mendelson JH, Sholar MB, Mutschler NH, Wines JD, Hesselbrock VM (2004) Brain alcohol detectability in human subjects with and without a paternal history of alcoholism. J Stud Alcohol 65(1):16–21

    PubMed  Google Scholar 

  27. 27.

    Fein G, Meyerhoff DJ (2000) Ethanol in human brain by magnetic resonance spectroscopy: correlation with blood and breath levels, relaxation, and magnetization transfer. Alcohol Clin Exp Res 24(8):1227–1235

    CAS  PubMed  Article  Google Scholar 

  28. 28.

    Kaufman MJ, Chiu TM, Mendelson JH, Woods BT, Teoh SK, Eros-Sarnyai M (1996) Brain alcohol detectability increase with repeated administration in humans: a proton spectroscopy study. Magn Reson Med 35(3):435–440

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Hanstock CC, Rothman DL, Shulman RG, Novotny EJ, Petroff OAC, Pritchard JW (1988) Ethanol observed in human brain by proton magnetic spectroscopy. Proc Soc Magn Reson Med (SMRM) 2:1071

    Google Scholar 

  30. 30.

    Hanstock CC, Rothman DL, Shulman RG, Novotny EJ Jr, Petroff OA, Prichard JW (1990) Measurement of ethanol in the human brain using NMR spectroscopy. J Stud Alcohol 51(2):104–107

    CAS  PubMed  Google Scholar 

  31. 31.

    Logsdail S, Miller D, Macmanus D, Johnson G, Lolin Y, O’Gorman P (1987) The effect of moderate blood alcohol levels on T1 and T2 relaxation times in the brains of normal volunteers. Magn Reson Med 4(4):378–379

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Mendelson J, Woods BT, Chiu TM, Mello NK, Lukas SE, Teoh SK (1990) Measurement of brain ethanol concentrations in humans with in vivo proton magnetic resonance spectroscopy. NIDA Res Monogr 105:68–74

    CAS  PubMed  Google Scholar 

  33. 33.

    Rooney WD, Lee JH, Li X, Wang GJ, Franceschi D, Springer CS Jr (2000) 4.0 T water proton T1 relaxation times in normal human brain and during acute ethanol intoxication. Alcohol Clin Exp Res 24(6):830–836

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30(6):672–679

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162–173

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Holmes CJ, Hoge R, Collins L, Woods R, Toga AW, Evans AC (1998) Enhancement of MR images using registration for signal averaging. J Comput Assist Tomogr 22(2):324–333

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Jang JH, Kim JH, Jung WH, Choi JS, Jung MH, Lee JM (2010) Functional connectivity in fronto-subcortical circuitry during the resting state in obsessive–compulsive disorder. Neurosci Lett 474(3):158–162

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Wang J, Wang L, Zang Y, Yang H, Tang H, Gong Q (2009) Parcellation-dependent small-world brain functional networks: a resting-state fMRI study. Hum Brain Mapp 30(5):1511–1523

    PubMed  Article  Google Scholar 

  39. 39.

    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(3):1178–1184

    PubMed  Article  Google Scholar 

  40. 40.

    Bassingthwaighte JB, Liebowitz LS, West BJ (1994) Fractal physiology. Oxford University Press, Oxford

    Book  Google Scholar 

  41. 41.

    Anderson CM, Lowen SB, Renshaw PF (2006) Emotional task-dependent low-frequency fluctuations and methylphenidate: wavelet scaling analysis of 1/f-type fluctuations in fMRI of the cerebellar vermis. J Neurosci Methods 151(1):52–61

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    De Graaf R (2007) In vivo NMR spectroscopy: principles and techniques, 2nd edn. Wiley, New York

    Book  Google Scholar 

  43. 43.

    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

    PubMed  Article  Google Scholar 

  44. 44.

    Field M, Wiers RW, Christiansen P, Fillmore MT, Verster JC (2010) Acute alcohol effects on inhibitory control and implicit cognition: implications for loss of control over drinking. Alcohol Clin Exp Res 34(8):1346–1352

    CAS  PubMed Central  PubMed  Google Scholar 

  45. 45.

    Steriade M, Llinas RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68(3):649–742

    CAS  PubMed  Google Scholar 

  46. 46.

    Stam CJ, de Haan W, Daffertshofer A, Jones BF, Manshanden I, van Cappellen van Walsum AM (2009) Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer’s disease. Brain 132(Pt 1):213–224

    CAS  PubMed  Google Scholar 

  47. 47.

    Warsi MA, Noseworthy MD (2011) Stability of brain resting state BOLD fractal dimension (FD) mapping. In: Proceedings of the 28th scientific meeting, European Society for Magnetic Resonance in Medicine and Biology (ESMRMB), Leipzig, Germany, p 512

  48. 48.

    Mathew RJ, Wilson WH (1986) Regional cerebral blood flow changes associated with ethanol intoxication. Stroke 17(6):1156–1159

    CAS  PubMed  Article  Google Scholar 

  49. 49.

    Newlin DB, Golden CJ, Quaife M, Graber B (1982) Effect of alcohol ingestion on regional cerebral blood flow. Int J Neurosci 17(3):145–150

    CAS  PubMed  Article  Google Scholar 

  50. 50.

    Volkow ND, Mullani N, Gould L, Adler SS, Guynn RW, Overall JE, Dewey S (1988) Effects of acute alcohol intoxication on cerebral blood flow measured with pet. Psychiatry Res 24(2):201–209

    CAS  PubMed  Article  Google Scholar 

  51. 51.

    Sano M, Wendt PE, Wirsen A, Stenberg G, Risberg J, Ingvar DH (1993) Acute effects of alcohol on regional cerebral blood flow in man. J Stud Alcohol 54(3):369–376

    CAS  PubMed  Google Scholar 

  52. 52.

    Tolentino NJ, Wierenga CE, Hall S, Tapert SF, Paulus MP, Liu TT, Smith TL, Schuckit MA (2011) Alcohol effects on cerebral blood flow in subjects with low and high responses to alcohol. Alcohol Clin Exp Res 35(6):1034–1040

    PubMed Central  PubMed  Article  Google Scholar 

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Acknowledgments

The work was funded by a postgraduate scholarship from the Natural Sciences and Engineering Research Council (NSERC) of Canada (AMW).

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Correspondence to Michael D. Noseworthy.

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Weber, A.M., Soreni, N. & Noseworthy, M.D. A preliminary study on the effects of acute ethanol ingestion on default mode network and temporal fractal properties of the brain. Magn Reson Mater Phy 27, 291–301 (2014). https://doi.org/10.1007/s10334-013-0420-5

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Keywords

  • MRI
  • MRS
  • BOLD
  • Ethanol
  • Resting state
  • Fractal dimension