Skip to main content
SpringerLink
Log in

Locally Measured Neuronal Correlates of Functional MRI Signals

  • Chapter
  • First Online:
EEG - fMRI

Abstract

Functional MRI (fMRI) utilizes changes in metabolic and hemodynamic signals in order to infer the underlying local changes in neuronal activity. fMRI signals are therefore an indirect measure of neuronal activity, with the involvement of intermediary processes of neurovascular coupling and MRI measurements. This chapter summarizes the current concepts surrounding the neuronal correlates of fMRI signals measured locally and the mechanisms by which neurovascular coupling is achieved.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science 273:1868–1871

    Article  PubMed  CAS  Google Scholar 

  • Arthurs OJ, Boniface SJ (2003) What aspect of the fMRI BOLD signal best reflects the underlying electrophysiology in human somatosensory cortex? Clin Neurophysiol 114:1203–1209

    Article  PubMed  CAS  Google Scholar 

  • Attwell D, Iadecola C (2002) The neural basis of functional brain imaging signals. Trends Neurosci 25:621–625

    Article  PubMed  CAS  Google Scholar 

  • Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS (1992) Time course EPI of human brain function during task activation. Magn Reson Med 25:390–397

    Article  PubMed  CAS  Google Scholar 

  • Birn RM, Diamond JB, Smith MA, Bandettini PA (2006) Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 31:1536–1548

    Article  PubMed  Google Scholar 

  • 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 34:537–541

    Article  PubMed  CAS  Google Scholar 

  • Braitenberg V, Schuz A (1991) Anatomy of the cortex. Springer, Berlin

    Google Scholar 

  • Brinker G, Bock C, Busch E, Krep H, Hossmann KA, Hoehn-Berlage M (1999) Simultaneous recording of evoked potentials and T2*-weighted MR images during somatosensory stimulation of rat. Magn Reson Med 41:469–473

    Article  PubMed  CAS  Google Scholar 

  • Buxton RB, Uludag K, Dubowitz DJ, Liu TT (2004) Modeling the hemodynamic response to brain activation. Neuroimage 23:S220–S233

    Article  PubMed  Google Scholar 

  • Cauli B, Tong XK, Rancillac A, Serluca N, Lambolez B, Rossier J, Hamel E (2004) Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci 24:8940–8949

    Article  PubMed  CAS  Google Scholar 

  • Cohen LB, De Weer P (1977) Structural and metabolic processes directly related to action potential propagation. In: Brookhart JM, Mountcastle VB (eds) Handbook of physiology: the nervous system. American Physiological Society, Bethesda, pp 137–159

    Google Scholar 

  • Cox SB, Woolsey TA, Rovainen CM (1993) Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J Cereb Blood Flow Metab 13:899–913

    Article  PubMed  CAS  Google Scholar 

  • Devor A, Dunn AK, Andermann ML, Ulbert I, Boas DA, Dale AM (2003) Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex. Neuron 39:353–359

    Article  PubMed  CAS  Google Scholar 

  • Devor A, Tian P, Nishimura N, Teng IC, Hillman EMC, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM (2007) Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J Neurosci 27:4452–4459

    Article  PubMed  CAS  Google Scholar 

  • Dietrich HH, Kajita T, Dacey RG (1996) Local and conducted vasomotor responses in isolated rat cerebral arterioles. Am J Physiol Heart Circ Physiol 271:H1109–H1116

    CAS  Google Scholar 

  • Duvernoy HM, Delon S, Vannson JL (1981) Cortical blood vessels of the human brain. Brain Res Bull 7:519–579

    Article  PubMed  CAS  Google Scholar 

  • Edvinsson L, Krause DN (eds) (2002) Cerebral blood flow and metabolism. Lippincott Williams and Wilkins, Philadelphia, pp 191–211

    Google Scholar 

  • Engel SA, Glover GH, Wandell BA (1997) Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex 7:181–192

    Article  PubMed  CAS  Google Scholar 

  • Faraci FM, Breese KR (1993) Nitric oxide mediates vasodilation in response to activation of N-methyl-d-aspartate receptors in brain. Circ Res 72:476–480

    Article  PubMed  CAS  Google Scholar 

  • Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711

    Article  PubMed  CAS  Google Scholar 

  • Fox PT, Raichle ME (1986) Focal physiological uncoupling of cerebral blood-flow and oxidative-metabolism during somatosensory stimulation in human-subjects. Proc Natl Acad Sci USA 83:1140–1144

    Article  PubMed  CAS  Google Scholar 

  • Freeman WJ (1975) Mass action in the nervous system. Academic, New York

    Google Scholar 

  • Girouard H, Iadecola C (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100:328–335

    Article  PubMed  CAS  Google Scholar 

  • Goense JBM, Logothetis NK (2008) Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol 18:631–640

    Article  PubMed  CAS  Google Scholar 

  • Hamel E (2004) Cholinergic modulation of the cortical microvascular bed. Prog Brain Res 145:171–178

    Article  PubMed  CAS  Google Scholar 

  • Harel N, Lee SP, Nagaoka T, Kim DS, Kim SG (2002) Origin of negative blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab 22:908–917

    Article  PubMed  Google Scholar 

  • Heeger DJ, Huk AC, Geisler WS, Albrecht DG (2000) Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? Nat Neurosci 3:631–633

    Article  PubMed  CAS  Google Scholar 

  • Heistad DD, Kontos HA (1983) Cerebral circulation. In: Shepherd JT, Abboud FM, Geiger SR (eds) Handbook of physiology, Sect 2, Vol III, Pt 1. The cardiovascular system. Circulation and organ blood flow (Chap 5). American Physiological Society, Bethesda, pp 137–182

    Google Scholar 

  • Hoffmeyer HW, Enager P, Thomsen KJ, Lauritzen MJ (2007) Nonlinear neurovascular coupling in rat sensory cortex by activation of transcallosal fibers. J Cereb Blood Flow Metab 27: 575–587

    Article  PubMed  Google Scholar 

  • Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB (1999) Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc Natl Acad Sci USA 96:9403–9408

    Article  PubMed  CAS  Google Scholar 

  • Iadecola C (1998) Cerebral circulatory dysregulation in ischemia. In: Ginsberg MD, Bogousslavsky J (eds) Cerebrovascular diseases. Blackwell Science, Cambridge, pp 319–332

    Google Scholar 

  • Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer’s disease. Nat Rev Neurosci 5:347–360

    Article  PubMed  CAS  Google Scholar 

  • Jones M, Hewson-Stoate N, Martindale J, Redgrave P, Mayhew J (2004) Nonlinear coupling of neural activity and CBF in rodent barrel cortex. Neuroimage 22:956–965

    Article  PubMed  Google Scholar 

  • Juergens E, Guettler A, Eckhorn R (1999) Visual stimulation elicits locked and induced gamma oscillations in monkey intracortical- and EEG-potentials, but not in human EEG. Exp Brain Res 129:247–259

    Article  PubMed  CAS  Google Scholar 

  • Kannurpatti SS, Biswal BB (2004) Negative functional response to sensory stimulation and its origins. J Cereb Blood Flow Metab 24:703–712

    Article  PubMed  Google Scholar 

  • Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, Kennedy DN, Hoppel BE, Cohen MS, Turner R, Cheng HM, Brady TJ, Rosen BR (1992) Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 89:5675–5679

    Article  PubMed  CAS  Google Scholar 

  • Lassen NA (1991) Cations as mediators of functional hyperemia in the brain. In: Lassen NA, Ingvar DH, Raichle ME, Friberg L (eds) Brain work and mental activity. Munksgaard, Copenhagen, pp 68–79

    Google Scholar 

  • Lauritzen M (2005) Reading vascular changes in brain imaging: is dendritic calcium the key? Nat Rev Neurosci 6:77–85

    Article  PubMed  CAS  Google Scholar 

  • Leopold DA, Murayama Y, Logothetis NK (2003) Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb Cortex 13:423–433

    Article  Google Scholar 

  • Logothetis NK (2002) The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci 357:1003–1037

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lou HC, Edvinsson L, MacKenzie ET (1987) The concept of coupling blood flow to brain function: revision required? Ann Neurol 22:289–297

    Article  PubMed  CAS  Google Scholar 

  • Mathiesen C, Caesar K, Akgoren N, Lauritzen M (1998) Modification of activity dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex. J Physiol 512:555–566

    Article  PubMed  CAS  Google Scholar 

  • Maunsell JH, Gibson JR (1992) Visual response latencies in striate cortex of the macaque monkey. J Neurophysiol 68:1332–1344

    PubMed  CAS  Google Scholar 

  • Mayhew JE, Askew S, Zheng Y, Porrill J, Westby GW, Redgrave P, Rector DM, Harper RM (1996) Cerebral vasomotion: a 0.1-Hz oscillation in reflected light imaging of neural activity. Neuroimage 4:183–193

    Article  PubMed  CAS  Google Scholar 

  • Mitzdorf U (1987) Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. Int J Neurosci 33:33–59

    Article  PubMed  CAS  Google Scholar 

  • Mukamel R, Gelbard H, Arieli A, Hasson U, Fried I, Malach R (2005) Coupling between neuronal firing, field potentials, and fMR1 in human auditory cortex. Science 309:951–954

    Article  PubMed  CAS  Google Scholar 

  • Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431:195–199

    Article  PubMed  CAS  Google Scholar 

  • Nicholson C (1973) Theoretical analysis of field potentials in anisotropic ensembles of neuronal elements. IEEE Trans Biomed Eng 20:278–288

    Article  PubMed  CAS  Google Scholar 

  • Nielsen A, Lauritzen M (2001) Coupling and uncoupling of activity-dependent increases of neuronal activity and blood flow in rat somatosensory cortex. J Physiol 533:773–785

    Article  CAS  Google Scholar 

  • Niessing J, Ebisch B, Schmidt KE, Niessing M, Singer W, Galuske RA (2005) Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309:948–951

    Article  PubMed  CAS  Google Scholar 

  • Nir Y, Fisch L, Mukamel R, Gelbard-Sagiv H, Arieli A, Fried I, Malach R (2007) Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr Biol 17:1275–1285

    Article  PubMed  CAS  Google Scholar 

  • Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87:9868–9872

    Article  PubMed  CAS  Google Scholar 

  • Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: Functional brain mapping with magnetic-resonance-imaging. Proc Natl Acad Sci USA 89:5951–5955

    Article  PubMed  CAS  Google Scholar 

  • Pasley BN, Inglis BA, Freeman RD (2007) Analysis of oxygen metabolism implies a neural origin for the negative BOLD response in human visual cortex. Neuroimage 36:269–276

    Article  PubMed  Google Scholar 

  • Pedemonte M, Barrenechea C, Nunez A, Gambini JP, Garcia-Austt E (1998) Membrane and circuit properties of lateral septum neurons: relationships with hippocampal rhythms. Brain Res 800:145–153

    Article  PubMed  CAS  Google Scholar 

  • Peters A, Payne BR (1993) Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex 3:69–78

    Article  PubMed  CAS  Google Scholar 

  • Peters A, Sethares CJ (1991) Organization of pyramidal neurons in area 17 of monkey visual cortex. J Comp Neurol 306:1–23

    Article  PubMed  CAS  Google Scholar 

  • Raichle ME, Mintum MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449–476

    Article  PubMed  CAS  Google Scholar 

  • Rauch A, Rainer G, Logothetis NK (2008) The effect of a serotonin-induced dissociation between spiking and perisynaptic activity on BOLD functional MRI. Proc Natl Acad Sci USA 105:6759–6764

    Article  PubMed  CAS  Google Scholar 

  • Rees G, Friston K, Koch C (2000) A direct quantitative relationship between the functional properties of human and macaque V5. Nat Neurosci 3:716–723

    Article  PubMed  CAS  Google Scholar 

  • Ritchie JM (1967) The oxygen consumption of mammalian non-myelinated nerve fibers at rest and during activity. J Physiol 188:309–329

    PubMed  CAS  Google Scholar 

  • Roy C, Sherrington C (1890) On the regulation of the blood supply of the brain. J Physiol 11:85–108

    PubMed  CAS  Google Scholar 

  • Saad ZS, Ropella KM, DeYoe EA, Bandettini PA (2003) The spatial extent of the BOLD response. Neuroimage 19:132–144

    Article  PubMed  Google Scholar 

  • Schwartz WJ, Smith CB, Davidsen L, Savaki H, Sokoloff L, et al. (1979) Metabolic mapping of functional activity in the hypothalamo-neurohypophysial system of the rat. Science 205:723–725

    Article  PubMed  CAS  Google Scholar 

  • Sheth SA, Nemoto M, Guiou M, Walker M, Pouratian N, Toga AW (2004) Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamic responses. Neuron 42:347–355

    Article  PubMed  CAS  Google Scholar 

  • Shmuel A, Augath M, Oeltermann A, Logothetis NK (2006) Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9:569–577

    Article  PubMed  CAS  Google Scholar 

  • Shmuel A, Grinvald A (1996) Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J Neurosci 16:6945–6964; and cover illustration

    PubMed  CAS  Google Scholar 

  • Shmuel A, Leopold DA (2008) Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest. Human Brain Mapp 29:751–761

    Article  Google Scholar 

  • Shmuel A, Yacoub E, Chaimow D, Logothetis NK, Ugurbil K (2007) Spatio-temporal point-spread function of fMRI signal in human gray matter at 7 Tesla. Neuroimage 35:539–552

    Article  PubMed  Google Scholar 

  • Shmuel A, Yacoub E, Pfeuffer J, Van de Moortele PF, Adriany G, Hu XP, Ugurbil K (2002) Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 36:1195–1210

    Article  PubMed  CAS  Google Scholar 

  • Smith AJ, Blumenfeld H, Behar KL, Rothman DL, Shulman RG, Hyder F (2002) Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc Natl Acad Sci USA 99:10765–10770

    Article  PubMed  CAS  Google Scholar 

  • Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, Sakurada O, Shinohara M (1977) The [14C] deoxyglucose method for the measurement of local glucose utilization: Theory, procedure and normal values in the conscious and anesthetized albino rat. J Neurochem 28:897–916

    Article  PubMed  CAS  Google Scholar 

  • Stefanovic B, Warnking JM, Kobayashi E, Bagshaw AP, Hawco C, Dubeau F, Gotman J, Pike GB (2005) Hemodynamic and metabolic responses to activation, deactivation and epileptic discharges. Neuroimage 28:205–215

    Article  PubMed  Google Scholar 

  • Stefanovic B, Warnking JM, Pike GB (2004) Hemodynamic and metabolic responses to neuronal inhibition. Neuroimage 22:771–778

    Article  PubMed  Google Scholar 

  • Thomsen K, Offenhauser N, Lauritzen M (2004) Principle neuron spiking: neither necessary nor sufficient for cerebral blood flow at rest or during activation in rat cerebellum. J Physiol 560:181–189

    Article  PubMed  CAS  Google Scholar 

  • UludaÄŸ K, Dubowitz DJ, Yoder EJ, Restom K, Liu TT, Buxton RB (2004) Coupling of cerebral blood flow and oxygen consumption during physiological activation and deactivation measured with fMRI. Neuroimage 23:148–155

    Article  PubMed  Google Scholar 

  • Viswanathan A, Freeman RD (2007) Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat Neurosci 10:1308–1312

    Article  PubMed  CAS  Google Scholar 

  • Wise RJS, Ide K, Poulin MJ, Tracey I (2004) Resting state fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 21:1652–1664

    Article  PubMed  Google Scholar 

  • Yang G, Huard JM, Beitz AJ, Ross ME, Iadecola C (2000) Stellate neurons mediate functional hyperemia in the cerebellar molecular layer. J Neurosci 20:6968–6973

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Montreal Neurological Institute, McGill University, Montreal, QC, Canada

    Amir Shmuel

Authors
  1. Amir Shmuel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amir Shmuel .

Editor information

Editors and Affiliations

  1. Psychiatrische Klinik, Universitätsklinikum München, Nußbaumstr. 7, München, 80336, Germany

    Christoph Mulert

  2. Inst. Neurology, University College London, Queen Square, London, WC1N 3BG, United Kingdom

    Louis Lemieux

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Shmuel, A. (2009). Locally Measured Neuronal Correlates of Functional MRI Signals. In: Mulert, C., Lemieux, L. (eds) EEG - fMRI. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-87919-0_4

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-87919-0_4

  • Published:

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-540-87918-3

  • Online ISBN: 978-3-540-87919-0

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation