SpringerLink
Log in

31P-MRS Using Visual Stimulation Protocols with Different Durations in Healthy Young Adult Subjects

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Phosphorus magnetic resonance spectroscopy (31P-MRS) combined with visual stimulation in functional experiments allows the non-invasive dynamic study of brain energy metabolism. 31P-MRS has been applied to several diseases and to healthy subjects, but works have shown variable findings and non-reproducible results, possibly caused by low numbers of subjects combined with different stimulation paradigms. In the present work, we used 31P-MRS at 3 T with two different visual stimulation protocols with different block duration (“short” and “long”) to evaluate metabolic changes under different workloads in 38 healthy subjects. We found a 15 % (short protocol—blocks of 1.5 min stimulation) and 3 % (long protocol—blocks of 5 min stimulation) increase in the inorganic phosphate (Pi) to α-adenosine triphosphate (α-ATP) ratio, and a 5 % (short protocol) and 2 % (long protocol) decrease in the nicotinamide adenine nucleotide (NADH + NAD+) to α-ATP ratio. The NADH + NAD+ results are, to the best of our knowledge, the first functional magnetic resonance spectroscopy in vivo assessment of these compounds, but their interpretation is difficult since they cannot be separately quantified at 3 T. Our results show that longer stimulations produce smaller concentration changes in Pi/α-ATP and (NADH + NAD+)/α-ATP ratios, which suggests a possible adaptation effect during longer stimulations that leads metabolic concentrations towards the initial equilibrium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Qiao H, Zhang X, Zhu X-H et al (2006) In vivo 31P MRS of human brain at high/ultrahigh fields: a quantitative comparison of NMR detection sensitivity and spectral resolution between 4 T and 7 T. Magn Reson Imaging 24:1281–1286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Nelson D, Cox M (2008) Lehninger principles of biochemistry, 5th edn. W.H. Freeman and Company, New York

    Google Scholar 

  3. Barker P, Butterworth E, Boska M et al (1999) Magnesium and pH imaging of the human brain at 3.0 Tesla. Magn Reson Med 41:400–406

    Article  CAS  PubMed  Google Scholar 

  4. Sappey-Marinier D, Calabrese G, Fein G et al (1992) Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 12:584–592

    Article  CAS  PubMed  Google Scholar 

  5. Rango M, Castelli A, Scarlato G (1997) Energetics of 3.5 s neural activation in humans: a 31P MR spectroscopy study. Magn Reson Med 38:878–883

    Article  CAS  PubMed  Google Scholar 

  6. Murashita J, Kato T, Shioiri T et al (1999) Age-dependent alteration of metabolic response to photic stimulation in the human brain measured by 31P MR-spectroscopy. Brain Res 818:72–76

    Article  CAS  PubMed  Google Scholar 

  7. Rango M, Bonifati C, Bresolin N (2006) Parkinson’s disease and brain mitochondrial dysfunction: a functional phosphorus magnetic resonance spectroscopy study. J Cereb Blood Flow Metab 26:283–290

    Article  CAS  PubMed  Google Scholar 

  8. Murashita J, Kato T, Shioiri T et al (2000) Altered brain energy metabolism in lithium-resistant bipolar disorder detected by photic stimulated 31P-MR spectroscopy. Psychol Med 30:107–115

    Article  CAS  PubMed  Google Scholar 

  9. Rango M, Bozzali M, Prelle A et al (2001) Brain activation in normal subjects and in patients affected by mitochondrial disease without clinical central nervous system involvement: a phosphorus magnetic resonance spectroscopy study. J Cereb Blood Flow Metab 21:85–91

    Article  CAS  PubMed  Google Scholar 

  10. Kato T, Murashita J, Shioiri T et al (1998) Photic stimulation-induced alteration of brain energy metabolism measured by 31P-MR spectroscopy in patients with MELAS. J Neurol Sci 155:182–185

    Article  CAS  PubMed  Google Scholar 

  11. Mochel F, N’Guyen T, Deelchand D et al (2012) Abnormal response to cortical activation in early stages of Huntington disease. Mov Disord 27:907–910

    Article  CAS  PubMed  Google Scholar 

  12. Kato T, Murashita J, Shioiri T et al (1996) Effect of photic stimulation on energy metabolism in the human brain measured by 31P-MR spectroscopy. J Neuropsychiatry Clin Neurosci 8:417–422

    CAS  PubMed  Google Scholar 

  13. Pipinos I, Shepard A, Anagnostopoulos P et al (2000) Phosphorus 31 nuclear magnetic resonance spectroscopy suggests a mitochondrial defect in claudicating skeletal muscle. J Vasc Surg 31:944–952

    Article  CAS  PubMed  Google Scholar 

  14. Longo R, Ricci C, Palma D et al (1993) Quantitative 31P MRS of the normal adult human brain. Assessment of interindividual differences and ageing effects. NMR Biomed 6:53–57

    Article  CAS  PubMed  Google Scholar 

  15. Petroff O, Prichard J, Behar K et al (1985) Cerebral intracellular pH by P-31 nuclear magnetic resonance spectroscopy. Neurology 35:781–788

    Article  CAS  PubMed  Google Scholar 

  16. Jeong E-K, Sung Y-H, Kim S-E et al (2011) Measurement of creatine kinase reaction rate in human brain using magnetization transfer image-selected in vivo spectroscopy (MT-ISIS) and a volume 31P/1H radiofrequency coil in a clinical 3-T MRI system. NMR Biomed 24:765–770

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Zhu X-H, Qiao H, Du F et al (2012) Quantitative imaging of energy expenditure in human brain. Neuroimage 60:2107–2117

    Article  PubMed Central  PubMed  Google Scholar 

  18. Chen W, Zhu X, Adriany G, Ugurbil K (1997) Increase of creatine kinase activity in the visual cortex of human brain during visual stimulation: a 31P magnetization transfer study. Magn Reson Med 38:551–557

    Article  CAS  PubMed  Google Scholar 

  19. Cadoux-Hudson T, Blackledge M, Radda G (1989) Imaging of human brain creatine kinase activity in vivo. FASEB J 3:2660–2666

    CAS  PubMed  Google Scholar 

  20. Vidyasagar R, Kauppinen R (2008) 31P magnetic resonance spectroscopy study of the human visual cortex during stimulation in mild hypoxic hypoxia. Exp Brain Res 187:229–235

    Article  PubMed  Google Scholar 

  21. Chen C, Gowland P, Francis S et al (2014) Assessing activation induced changes in creatine kinase activity in the human brain using 31P spectroscopy with magnetization transfer. In: Proceedings 22nd scientific meeting and exhibition international society for magnetic resonance in medicine 462

  22. Lee B, Zhu X-H, Chen W (2014) Elevated ATP synthase and creatine kinase activities in human visual cortex during visual stimulation: a 31P NMR magnetization transfer study at 7 T. In: Proceedings 22nd scientific meeting and exhibition international society for magnetic resonance in medicine 0012

  23. Lin A-L, Fox PT, Hardies J et al (2010) Nonlinear coupling between cerebral blood flow, oxygen consumption, and ATP production in human visual cortex. Proc Natl Acad Sci USA 107:8446–8451

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Frahm J, Krüger G, Merboldt K, Kleinschmidt A (1996) Dynamic uncoupling and recoupling of perfusion and oxidative metabolism during focal brain activation in man. Magn Reson Med 35:143–148

    Article  CAS  PubMed  Google Scholar 

  25. Kasischke K, Vishwasrao H, Fisher P et al (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305(5680):99–103

    Article  CAS  PubMed  Google Scholar 

  26. Hall C, Klein-Flugge M, Howarth C, Attwell D (2012) Oxidative phosphorylation, not glycolisys, powers presynaptic and postsynaptic mechanisms underlying brain information processing. J Neurosci 32:8940–8951

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412(6843):150–157

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil—Grants 2005/56578-4, 2009/00270-2, 2009/10046-2, 2011/01106-1) and Conselho Nacional de Pesquisa (CNPq, Brazil—Grant 500148/2011-2).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Physics, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes 3900, Monte Alegre, Ribeirão Preto, SP, 14040901, Brazil

    Felipe R. Barreto & Carlos E. G. Salmon

  2. Neurophysics Group, Departamento de Cronologia, Instituto de Física Gleb Wataghin, Raios Cósmicos, Altas Energias e Léptons, Universidade de Campinas (UNICAMP), Rua Sérgio Buarque de Holanda 777, Cidade Universitária, Campinas, SP, 13083859, Brazil

    Thiago B. S. Costa, Ricardo C. G. Landim & Gabriela Castellano

  3. CInAPCe Program (Cooperação Interinstitucional de Apoio a Pesquisas sobre o Cérebro), São Paulo, Brazil

    Felipe R. Barreto, Thiago B. S. Costa, Ricardo C. G. Landim, Gabriela Castellano & Carlos E. G. Salmon

Authors
  1. Felipe R. Barreto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thiago B. S. Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricardo C. G. Landim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriela Castellano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carlos E. G. Salmon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carlos E. G. Salmon.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barreto, F.R., Costa, T.B.S., Landim, R.C.G. et al. 31P-MRS Using Visual Stimulation Protocols with Different Durations in Healthy Young Adult Subjects. Neurochem Res 39, 2343–2350 (2014). https://doi.org/10.1007/s11064-014-1433-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-014-1433-9

Keywords

Search

Navigation