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.
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.54.1.135Search 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)00038-2Search 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/nature09613Search 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-XSearch 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/BF03206846Search 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.6063-09.2010Search 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, 366–371.10.1080/10903120802100100Search 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.2009.11.007Search 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/BF03207059Search 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/BF03211893Search 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.0407789102Search 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.0134-07.2007Search 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/BF03206719Search 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.xSearch 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, 1071–1079.10.1162/089892901753294365Search 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, 908–917.10.1097/00004647-200208000-00002Search 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.1999.0470Search 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.5536-05.2006Search 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.2014.04.022Search in Google Scholar PubMed
Iadecola, C. and Nedergaard, M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369–1376.10.1038/nn2003Search in Google Scholar PubMed
Iwamura, Y., Iriki, A., and Tanaka, M. (1994). Bilateral hand representation in the postcentral somatosensory cortex. Nature 369, 554–556.10.1038/369554a0Search in Google Scholar PubMed
Iwamura, Y., Taoka, M., and Iriki, A. (2001). Bilateral activity and callosal connections in the somatosensory cortex. Neuroscientist 7, 419–429.10.1177/107385840100700511Search 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.2008.03.049Search 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.902190403Search 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.2010.05.087Search 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.2011.01.028Search 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.21006Search 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.22163Search 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.2008.11.005Search 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/bhq151Search 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.2004.10.018Search 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, 150–157.10.1038/35084005Search 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.Search 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/s11682-014-9302-3Search 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.2004.10.011Search 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.89.13.5951Search 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.2006.09.015Search 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.2009.188Search 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/BF03209769Search 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.2011.11.085Search in Google Scholar PubMed
Schnitzler, A. and Ploner, M. (2000). Neurophysiology and functional neuroanatomy of pain perception. J. Clin. Neurophysiol. 17, 592–603.10.1097/00004691-200011000-00005Search 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.21203Search 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)01061-9Search 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/nn1675Search 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.20017Search 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.2004.01.036Search 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.2006.08.015Search in Google Scholar PubMed
Thompson, R.F. (2009). Habituation: a history. Neurobiol. Learn. Mem. 92, 127–134.10.1016/j.nlm.2008.07.011Search 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/h0022681Search 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/Y09-048Search 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.2007.05.002Search in Google Scholar PubMed
©2015 by De Gruyter
Articles in the same Issue
- Frontmatter
- Magnetic resonance spectroscopy of the brain: a review of physical principles and technical methods
- The utility of fractal analysis in clinical neuroscience
- The importance of the negative blood-oxygenation-level-dependent (BOLD) response in the somatosensory cortex
- Electric foot shock stress: a useful tool in neuropsychiatric studies
- Tryptophan hydroxylase 2 in seasonal affective disorder: underestimated perspectives?
- Receptor for advanced glycation end-products in neurodegenerative diseases
- Phytochemical constituents as future antidepressants: a comprehensive review
- Spotting psychopaths using technology
Articles in the same Issue
- Frontmatter
- Magnetic resonance spectroscopy of the brain: a review of physical principles and technical methods
- The utility of fractal analysis in clinical neuroscience
- The importance of the negative blood-oxygenation-level-dependent (BOLD) response in the somatosensory cortex
- Electric foot shock stress: a useful tool in neuropsychiatric studies
- Tryptophan hydroxylase 2 in seasonal affective disorder: underestimated perspectives?
- Receptor for advanced glycation end-products in neurodegenerative diseases
- Phytochemical constituents as future antidepressants: a comprehensive review
- Spotting psychopaths using technology