Startseite The importance of the negative blood-oxygenation-level-dependent (BOLD) response in the somatosensory cortex
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The importance of the negative blood-oxygenation-level-dependent (BOLD) response in the somatosensory cortex

  • Carsten M. Klingner EMAIL logo , Stefan Brodoehl und Otto W. Witte
Veröffentlicht/Copyright: 9. Juni 2015
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Abstract

In recent years, multiple studies have shown task-induced negative blood-oxygenation-level-dependent responses (NBRs) in multiple brain regions in humans and animals. Converging evidence suggests that task-induced NBRs can be interpreted in terms of decreased neuronal activity. However, the vascular and metabolic dynamics and functional importance of the NBR are highly debated. Here, we review studies investigating the origin and functional importance of the NBR, with special attention to the somatosensory cortex.


Corresponding author: Carsten M. Klingner, Hans Berger Clinic for Neurology, University Hospital Jena, Friedrich Schiller University, Erlanger Allee 101, D-07747 Jena, Germany, e-mail:

References

Allison, J.D., Meador, K.J., Loring, D.W., Figueroa, R.E., and Wright, J.C. (2000). Functional MRI cerebral activation and deactivation during finger movement. Neurology 54, 135–142.10.1212/WNL.54.1.135Suche in Google Scholar

Ames, A. 3rd (2000). CNS energy metabolism as related to function. Brain Res. Brain Res. Rev. 34, 42–68.10.1016/S0165-0173(00)00038-2Suche in Google Scholar

Attwell, D., Buchan, A.M., Charpak, S., Lauritzen, M., Macvicar, B.A., and Newman, E.A. (2010). Glial and neuronal control of brain blood flow. Nature 468, 232–243.10.1038/nature09613Suche in Google Scholar

Backes, W.H., Mess, W.H., van Kranen-Mastenbroek, V., and Reulen, J.P. (2000). Somatosensory cortex responses to median nerve stimulation: fMRI effects of current amplitude and selective attention. Clin. Neurophysiol. 111, 1738–1744.10.1016/S1388-2457(00)00420-XSuche in Google Scholar

Ballesteros, S., Manga, D., and Reales, J.M. (1997). Haptic discrimination of bilateral symmetry in 2-dimensional and 3-dimensional unfamiliar displays. Percept. Psychophys. 59, 37–50.10.3758/BF03206846Suche in Google Scholar PubMed

Boorman, L., Kennerley, A.J., Johnston, D., Jones, M., Zheng, Y., Redgrave, P., and Berwick, J. (2010). Negative blood oxygen level dependence in the rat: a model for investigating the role of suppression in neurovascular coupling. J. Neurosci. 30, 4285–4294.10.1523/JNEUROSCI.6063-09.2010Suche in Google Scholar PubMed PubMed Central

Brice, J.H., Evenson, K.R., Lellis, J.C., Rosamond, W.D., Aytur, S.A., Christian, J.B., and Morris, D.L. (2008). Emergency medical services education, community outreach, and protocols for stroke and chest pain in North Carolina. Prehosp. Emerg. Care 12, 366–371.10.1080/10903120802100100Suche in Google Scholar PubMed

Carmignoto, G. and Gomez-Gonzalo, M. (2010). The contribution of astrocyte signalling to neurovascular coupling. Brain Res. Rev. 63, 138–148.10.1016/j.brainresrev.2009.11.007Suche in Google Scholar PubMed

Craig, J.C. (1985). Attending to two fingers: two hands are better than one. Percept. Psychophys. 38, 496–511.10.3758/BF03207059Suche in Google Scholar

Craig, J.C. and Qian, X. (1997). Tactile pattern perception by two fingers: temporal interference and response competition. Percept. Psychophys. 59, 252–265.10.3758/BF03211893Suche in Google Scholar

Devor, A., Ulbert, I., Dunn, A.K., Narayanan, S.N., Jones, S.R., Andermann, M.L., Boas, D.A., and Dale, A.M. (2005). Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity. Proc. Natl. Acad. Sci. USA 102, 3822–3827.10.1073/pnas.0407789102Suche in Google Scholar PubMed PubMed Central

Devor, A., Tian, P., Nishimura, N., Teng, I.C., Hillman, E.M., Narayanan, S.N., Ulbert, I., Boas, D.A., Kleinfeld, D., and Dale, A.M. (2007). Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J. Neurosci. 27, 4452–4459.10.1523/JNEUROSCI.0134-07.2007Suche in Google Scholar PubMed PubMed Central

Evans, P.M., Craig, J.C., and Rinker, M.A. (1992). Perceptual processing of adjacent and nonadjacent tactile nontargets. Percept. Psychophys. 52, 571–581.10.3758/BF03206719Suche in Google Scholar PubMed

Fabri, M., Polonara, G., Quattrini, A., Salvolini, U., Del Pesce, M., and Manzoni, T. (1999). Role of the corpus callosum in the somatosensory activation of the ipsilateral cerebral cortex: an fMRI study of callosotomized patients. Eur. J. Neurosci. 11, 3983–3994.10.1046/j.1460-9568.1999.00829.xSuche in Google Scholar PubMed

Fabri, M., Polonara, G., Del Pesce, M., Quattrini, A., Salvolini, U., and Manzoni, T. (2001). Posterior corpus callosum and interhemispheric transfer of somatosensory information: an fMRI and neuropsychological study of a partially callosotomized patient. J. Cognit. Neurosci. 13, 1071–1079.10.1162/089892901753294365Suche in Google Scholar PubMed

Harel, N., Lee, S.P., Nagaoka, T., Kim, D.S., and Kim, S.G. (2002). Origin of negative blood oxygenation level-dependent fMRI signals. J. Cereb. Blood Flow Metab. 22, 908–917.10.1097/00004647-200208000-00002Suche in Google Scholar PubMed

Hari, R. and Forss, N. (1999). Magnetoencephalography in the study of human somatosensory cortical processing. Philos. Trans. R. Soc. Lond. 354, 1145–1154.10.1098/rstb.1999.0470Suche in Google Scholar PubMed PubMed Central

Hlushchuk, Y. and Hari, R. (2006). Transient suppression of ipsilateral primary somatosensory cortex during tactile finger stimulation. J. Neurosci. 26, 5819–5824.10.1523/JNEUROSCI.5536-05.2006Suche in Google Scholar PubMed PubMed Central

Huber, L., Goense, J., Kennerley, A.J., Ivanov, D., Krieger, S.N., Lepsien, J., Trampel, R., Turner, R., and Moller, H.E. (2014). Investigation of the neurovascular coupling in positive and negative BOLD responses in human brain at 7T. Neuroimage 97, 349–362.10.1016/j.neuroimage.2014.04.022Suche in Google Scholar PubMed

Iadecola, C. and Nedergaard, M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369–1376.10.1038/nn2003Suche in Google Scholar PubMed

Iwamura, Y., Iriki, A., and Tanaka, M. (1994). Bilateral hand representation in the postcentral somatosensory cortex. Nature 369, 554–556.10.1038/369554a0Suche in Google Scholar PubMed

Iwamura, Y., Taoka, M., and Iriki, A. (2001). Bilateral activity and callosal connections in the somatosensory cortex. Neuroscientist 7, 419–429.10.1177/107385840100700511Suche in Google Scholar PubMed

Kastrup, A., Baudewig, J., Schnaudigel, S., Huonker, R., Becker, L., Sohns, J.M., Dechent, P., Klingner, C., and Witte, O.W. (2008). Behavioral correlates of negative BOLD signal changes in the primary somatosensory cortex. Neuroimage 41, 1364–1371.10.1016/j.neuroimage.2008.03.049Suche in Google Scholar PubMed

Killackey, H.P., Gould, H.J. 3rd, Cusick, C.G., Pons, T.P., and Kaas, J.H. (1983). The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys. J. Comp. Neurol. 219, 384–419.10.1002/cne.902190403Suche in Google Scholar PubMed

Klingner, C.M., Hasler, C., Brodoehl, S., and Witte, O.W. (2010). Dependence of the negative BOLD response on somatosensory stimulus intensity. Neuroimage 53, 189–195.10.1016/j.neuroimage.2010.05.087Suche in Google Scholar PubMed

Klingner, C.M., Ebenau, K., Hasler, C., Brodoehl, S., Gorlich, Y., and Witte, O.W. (2011a). Influences of negative BOLD responses on positive BOLD responses. Neuroimage 55, 1709–1715.10.1016/j.neuroimage.2011.01.028Suche in Google Scholar PubMed

Klingner, C.M., Huonker, R., Flemming, S., Hasler, C., Brodoehl, S., Preul, C., Burmeister, H., Kastrup, A., and Witte, O.W. (2011b). Functional deactivations: multiple ipsilateral brain areas engaged in the processing of somatosensory information. Hum. Brain Mapp. 32, 127–140.10.1002/hbm.21006Suche in Google Scholar PubMed PubMed Central

Klingner, C.M., Hasler, C., Brodoehl, S., and Witte, O.W. (2014). Excitatory and inhibitory mechanisms underlying somatosensory habituation. Hum. Brain Mapp. 35, 152–160.10.1002/hbm.22163Suche in Google Scholar PubMed PubMed Central

Koehler, R.C., Roman, R.J., and Harder, D.R. (2009). Astrocytes and the regulation of cerebral blood flow. Trends Neurosci. 32, 160–169.10.1016/j.tins.2008.11.005Suche in Google Scholar PubMed

Lin, P., Hasson, U., Jovicich, J., and Robinson, S. (2011). A neuronal basis for task-negative responses in the human brain. Cereb. Cortex. 21, 821–830.10.1093/cercor/bhq151Suche in Google Scholar PubMed PubMed Central

Logothetis, N.K. and Pfeuffer, J. (2004). On the nature of the BOLD fMRI contrast mechanism. Magn. Reson. Imaging 22, 1517–1531.10.1016/j.mri.2004.10.018Suche in Google Scholar PubMed

Logothetis, N.K., Pauls, J., Augath, M., Trinath, T., and Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 150–157.10.1038/35084005Suche in Google Scholar PubMed

Maggioni, E., Molteni, E., Arrigoni, F., Zucca, C., Reni, G., Triulzi, F.M., and Bianchi, A.M. (2013). Coupling of fMRI and NIRS measurements in the study of negative BOLD response to intermittent photic stimulation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2013, 1378–1381.Suche in Google Scholar

McGregor, K.M., Sudhyadhom, A., Nocera, J., Seff, A., Crosson, B., and Butler, A.J. (2014). Reliability of negative BOLD in ipsilateral sensorimotor areas during unimanual task activity. Brain Imaging Behav. 9, 245–254.10.1007/s11682-014-9302-3Suche in Google Scholar PubMed

Nihashi, T., Naganawa, S., Sato, C., Kawai, H., Nakamura, T., Fukatsu, H., Ishigaki, T., and Aoki, I. (2005). Contralateral and ipsilateral responses in primary somatosensory cortex following electrical median nerve stimulation – an fMRI study. Clin. Neurophysiol. 116, 842–848.10.1016/j.clinph.2004.10.011Suche in Google Scholar PubMed

Ogawa, S., Tank, D.W., Menon, R., Ellermann, J.M., Kim, S.G., Merkle, H., and Ugurbil, K. (1992). Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 89, 5951–5955.10.1073/pnas.89.13.5951Suche in Google Scholar PubMed PubMed Central

Pasley, B.N., Inglis, B.A., and Freeman, R.D. (2007). Analysis of oxygen metabolism implies a neural origin for the negative BOLD response in human visual cortex. Neuroimage 36, 269–276.10.1016/j.neuroimage.2006.09.015Suche in Google Scholar PubMed PubMed Central

Paulson, O.B., Hasselbalch, S.G., Rostrup, E., Knudsen, G.M., and Pelligrino, D. (2010). Cerebral blood flow response to functional activation. J. Cereb. Blood Flow Metab. 30, 2–14.10.1038/jcbfm.2009.188Suche in Google Scholar PubMed PubMed Central

Rinker, M.A. and Craig, J.C. (1994). The effect of spatial orientation on the perception of moving tactile stimuli. Percept. Psychophys. 56, 356–362.10.3758/BF03209769Suche in Google Scholar PubMed

Schafer, K., Blankenburg, F., Kupers, R., Gruner, J.M., Law, I., Lauritzen, M., and Larsson, H.B. (2012). Negative BOLD signal changes in ipsilateral primary somatosensory cortex are associated with perfusion decreases and behavioral evidence for functional inhibition. Neuroimage 59, 3119–3127.10.1016/j.neuroimage.2011.11.085Suche in Google Scholar PubMed

Schnitzler, A. and Ploner, M. (2000). Neurophysiology and functional neuroanatomy of pain perception. J. Clin. Neurophysiol. 17, 592–603.10.1097/00004691-200011000-00005Suche in Google Scholar PubMed

Shen, Q., Ren, H., and Duong, T.Q. (2008). CBF, BOLD, CBV, and CMRO(2) fMRI signal temporal dynamics at 500-msec resolution. J. Magn. Reson. Imaging 27, 599–606.10.1002/jmri.21203Suche in Google Scholar

Shmuel, A., Yacoub, E., Pfeuffer, J., Van de Moortele, P.F., Adriany, G., Hu, X., and 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, 1195–1210.10.1016/S0896-6273(02)01061-9Suche in Google Scholar

Shmuel, A., Augath, M., Oeltermann, A., and Logothetis, N.K. (2006). Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat. Neurosci. 9, 569–577.10.1038/nn1675Suche in Google Scholar PubMed

Smith, A.T., Williams, A.L., and Singh, K.D. (2004). Negative BOLD in the visual cortex: evidence against blood stealing. Hum. Brain Mapp. 21, 213–220.10.1002/hbm.20017Suche in Google Scholar PubMed PubMed Central

Stefanovic, B., Warnking, J.M., and Pike, G.B. (2004). Hemodynamic and metabolic responses to neuronal inhibition. Neuroimage 22, 771–778.10.1016/j.neuroimage.2004.01.036Suche in Google Scholar PubMed

Sutherland, M.T. and Tang, A.C. (2006). Reliable detection of bilateral activation in human primary somatosensory cortex by unilateral median nerve stimulation. Neuroimage 33, 1042–1054.10.1016/j.neuroimage.2006.08.015Suche in Google Scholar PubMed

Thompson, R.F. (2009). Habituation: a history. Neurobiol. Learn. Mem. 92, 127–134.10.1016/j.nlm.2008.07.011Suche in Google Scholar PubMed PubMed Central

Thompson, R.F. and Spencer, W.A. (1966). Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 73, 16–43.10.1037/h0022681Suche in Google Scholar PubMed

Toda, N., Ayajiki, K., and Okamura, T. (2009). Cerebral blood flow regulation by nitric oxide in neurological disorders. Can. J. Physiol. Pharmacol. 87, 581–594.10.1139/Y09-048Suche in Google Scholar PubMed

Zhang, N., Gore, J.C., Chen, L.M., and Avison, M.J. (2007). Dependence of BOLD signal change on tactile stimulus intensity in SI of primates. Magn. Reson. Imaging 25, 784–794.10.1016/j.mri.2007.05.002Suche in Google Scholar PubMed

Received: 2015-1-22
Accepted: 2015-4-17
Published Online: 2015-6-9
Published in Print: 2015-12-1

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