Prediction of Task-Related BOLD fMRI with Amplitude Signatures of Resting-State fMRI

Sridhar S Kannurpatti, Bart Rypma, Bharat B Biswal, Sridhar S Kannurpatti, Bart Rypma, Bharat B Biswal

Abstract

Blood oxygen contrast-functional magnetic resonance imaging (fMRI) signals are a convolution of neural and vascular components. Several studies indicate that task-related (T-fMRI) or resting-state (R-fMRI) responses linearly relate to hypercapnic task responses. Based on the linearity of R-fMRI and T-fMRI with hypercapnia demonstrated by different groups using different study designs, we hypothesized that R-fMRI and T-fMRI signals are governed by a common physiological mechanism and that resting-state fluctuation of amplitude (RSFA) should be linearly related to T-fMRI responses. We tested this prediction in a group of healthy younger humans where R-fMRI, T-fMRI, and hypercapnic (breath hold, BH) task measures were obtained form the same scan session during resting state and during performance of motor and BH tasks. Within individual subjects, significant linear correlations were observed between motor and BH task responses across voxels. When averaged over the whole brain, the subject-wise correlation between the motor and BH tasks showed a similar linear relationship within the group. Likewise, a significant linear correlation was observed between motor-task activity and RSFA across voxels and subjects. The linear rest-task (R-T) relationship between motor activity and RSFA suggested that R-fMRI and T-fMRI responses are governed by similar physiological mechanisms. A practical use of the R-T relationship is its potential to estimate T-fMRI responses in special populations unable to perform tasks during fMRI scanning. Using the R-T relationship determined from the first group of 12 healthy subjects, we predicted the T-fMRI responses in a second group of 7 healthy subjects. RSFA in both the lower and higher frequency ranges robustly predicted the magnitude of T-fMRI responses at the subject and voxel levels. We propose that T-fMRI responses are reliably predictable to the voxel level in situations where only R-fMRI measures are possible, and may be useful for assessing neural activity in task non-compliant clinical populations.

Keywords: BOLD; breath hold; fMRI; hypercapnia; motor cortex; prediction; resting-state fluctuations; vascular.

Figures

Figure 1
Figure 1
Estimation of the BOLD amplitude change during the resting state (top) and task (bottom) using the temporal SD of the time series.
Figure 2
Figure 2
Spatiotemporal structure of the BOLD amplitude change (SD) from the motor-task region of interest (ROI). (A–C) Spatial and (D–I) temporal. (A) Resting state, (B) motor task, and (C) BH task. Voxels with large RSFA also tend to have large BOLD amplitude change during the motor and BH tasks. Such a spatial correspondence between R-fMRI, T-fMRI, and hypercapnia was observed over all subjects. (Different color scales have been used to visually normalize the color maps across the different experimental conditions). (D–F) BOLD signal time courses of the R-fMRI, T-fMRI, and hypercapnia respectively from a typical gray matter voxel within the motor-task ROI. (G–I) BOLD signal time courses of the R-fMRI, T-fMRI, and hypercapnia respectively from a typical white matter voxel within the motor-task ROI.
Figure 3
Figure 3
(A) Voxel-level relationship between motor vs BH (r = 0.91; P < 10−7) and (B) motor vs RSFA (r = 0.84; P < 10−7). Voxels were derived after cross correlating the BOLD response time courses with the gamma-variate convolved motor-task reference vector. Voxels with cross-correlation coefficient (cc) ≥0.7 corresponding to a Bonferroni corrected P < 10−5 was used to generate the correlations. Plots are representative of a typical subject.
Figure 4
Figure 4
Voxel-wise relationship between R-fMRI, T-fMRI, and hypercapnic (BH) responses in a typical subject. (A) Low frequency RSFA vs motor task (r = 0.82; P < 10−8), (B) high frequency RSFA vs motor task (r = 0.67; P < 10−8), (C) low frequency RSFA vs BH (r = 0.88; P < 10−8), and (D) high frequency RSFA vs BH (r = 0.66; P < 10−8).
Figure 5
Figure 5
Subject-wise relationship between R-fMRI, T-fMRI and hypercapnic (BH) responses. (A) T-fMRI vs BH (r = 0.57; P < 0.04), (B) T-fMRI vs low frequency RSFA (r = 0.50; P < 0.05), and (C) T-fMRI vs high frequency RSFA (r = 0.58; P < 0.04). A strong linear relationship was observed from the voxel-averaged BOLD signals at the subject level. The relationships shown in (B) and (C) were subsequently used to predict T-fMRI responses from a second group of subjects scanned at a different site.
Figure 6
Figure 6
Subject-wise relationship of the low and high frequency components of RSFA between themselves and BH. (A) High frequency RSFA vs low frequency RSFA (r = 0.67; P < 0.02), (B) BH vs high frequency RSFA (r = 0.51; P < 0.05), and (C) BH vs low frequency RSFA (r = 0.70; P < 0.01). A strong linear relationship was observed from the voxel-averaged BOLD signals at the subject level. The relationship indicates a significantly higher vascular component in the low frequency RSFA compared to high frequency RSFA.
Figure 7
Figure 7
Predicted volume of the motor-task activated ROI with an accuracy of (A) 90% and above, (B) 75% and above. T-fMRI responses across voxels were predicted using the subject-wise R–T relationship in the low and high frequency RSFA derived from the first group of subjects. *Significantly different with respect to low frequency RSFA; paired t-test, P < 0.02. **Significantly different with respect to high frequency RSFA; paired t-test, P < 0.001.

References

    1. Bandettini P. A., Jesmanowicz A., Wong E. C., Hyde J. S. (1993). Processing strategies for the time-course data sets in fMRI of the human brain. Magn. Reson. Med. 30, 161–173.10.1002/mrm.1910300204
    1. Birn R. M., Diamond J. B., Smith M. A., Bandettini P. A. (2006). Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 31, 1536–1548.10.1016/j.neuroimage.2006.02.048
    1. Biswal B., Yetkin F. Z., Haughton V. M., Hyde J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537–541.10.1002/mrm.1910340409
    1. Biswal B. B., Eldreth D. A., Motes M. A., Rypma B. (2010). Task-dependent individual differences in prefrontal connectivity. Cereb. Cortex 20, 2188–2197.10.1093/cercor/bhp284
    1. Biswal B. B., Kannurpatti S. S., Rypma B. (2007). Hemodynamic scaling of fMRI-BOLD signal: validation of low-frequency spectral amplitude as a scalability factor. Magn. Reson. Imaging 25, 1358–1369.10.1016/j.mri.2007.03.022
    1. Boxerman J. L., Bandettini P. A., Kwong K. K., Baker J. R., Davis T. L., Rosen B. R., Weisskoff R. M. (1995). The intravascular contribution to fMRI signal change: Monte Carlo modeling and diffusion-weighted studies in vivo. Magn. Reson. Med. 34, 4–10.10.1002/mrm.1910340103
    1. Chang C., Glover G. H. (2009). Relationship between respiration, end-tidal CO2, and BOLD signals in resting-state fMRI. Neuroimage 47, 1381–1393.10.1016/S1053-8119(09)70777-3
    1. Cordes D., Haughton V. M., Arfanakis K., Wendt G. J., Turski P. A., Moritz C. H., Quigley M. A., Meyerand M. E. (2000). Mapping functionally related regions of brain with functional connectivity MR imaging. AJNR Am. J. Neuroradiol. 21, 1636–1644.
    1. Cox R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162–173.10.1006/cbmr.1996.0014
    1. Dagli M. S., Ingeholm J. E., Haxby J. V. (1999). Localization of cardiac-induced signal change in fMRI. Neuroimage 9, 407–415.10.1006/nimg.1998.0424
    1. Damoiseaux J. S., Rombouts S. A., Barkhof F., Scheltens P., Stam C. J., Smith S. M., Beckmann C. F. (2006). Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U.S.A. 103, 13848–13853.10.1073/pnas.0601417103
    1. Davis T., Kwong K., Weisskoff R., Rosen B. R. (1998). Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. U.S.A. 95, 1834–1839.10.1073/pnas.95.1.78
    1. Fox M. D., Snyder A. Z., Vincent J. L., Corbetta M., Van Essen D. C., Raichle M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A. 102, 9673–9678.10.1073/pnas.0504136102
    1. Fox M. D., Raichle M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700–711.10.1038/nrn2201
    1. Greicius M. D., Srivastava G., Reiss A. L., Menon V. (2004). Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U.S.A. 101, 4637–4642.10.1073/pnas.0308627101
    1. Handwerker D. A., Gazzaley A., Inglis B. A., D’Esposito M. (2007). Reducing vascular variability of fMRI data across aging populations using a breathholding task. Hum. Brain Mapp. 28, 846–859.10.1002/hbm.20307
    1. Hoge R. D., Atkinson J., Gill B., Crelier G. R., Marrett S., Pike G. B. (1999). Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn. Reson. Med. 42, 849–863.10.1002/(SICI)1522-2594(199911)42:5<849::AID-MRM4>;2-Z
    1. Hoge R. D., Pike G. B. (2001). Oxidative metabolism and the detection of neuronal activation via imaging. J. Chem. Neuroanat. 22, 43–52.10.1016/S0891-0618(01)00114-4
    1. Hyder F., Rothman D. L. (2010). Neuronal correlate of BOLD signal fluctuations at rest: err on the side of the baseline. Proc. Natl. Acad. Sci. U.S.A. 107, 10773–10774.10.1073/pnas.1005135107
    1. Hyder F., Rothman D. L. (2011). Evidence for the importance of measuring total brain activity in neuroimaging. Proc. Natl. Acad. Sci. U.S.A. 108, 5475–5476.10.1073/pnas.1102026108
    1. Jiang A., Kennedy D. N., Baker J. R., Weisskoff R. M., Tootell R. B. H., Woods R. P., Benson R. R., Kwong K. K., Brady T. J., Rosen B. R., Belliveau J. W. (1995). Motion detection and correction in functional MR imaging. Hum. Brain Mapp. 3, 224–23510.1002/hbm.460030306
    1. Jo H. J., Saad Z. S., Simmons W. K., Milbury L. A., Cox R. W. (2010). Mapping sources of correlation in resting state FMRI, with artifact detection and removal. Neuroimage 52, 571–582.10.1016/j.neuroimage.2010.04.246
    1. Kannurpatti S. S., Biswal B. B. (2008). Detection and scaling of task-induced fMRI-BOLD response using resting state fluctuations. Neuroimage 40, 1567–1574.10.1016/j.neuroimage.2007.05.061
    1. Kannurpatti S. S., Biswal B. B., Hudetz A. G. (2002). Differential fMRI-BOLD signal response to apnea in humans and anesthetized rats. Magn. Reson. Med. 47, 864–870.10.1002/mrm.10131
    1. Kannurpatti S. S., Biswal B. B., Kim Y. R., Rosen B. R. (2008). Spatio-temporal characteristics of low-frequency BOLD signal fluctuations in isoflurane-anesthetized rat brain. Neuroimage 40, 1738–1747.10.1016/j.neuroimage.2007.05.061
    1. Kannurpatti S. S., Motes M. A., Rypma B., Biswal B. B. (2011). Increasing measurement accuracy of age-related BOLD signal change: minimizing vascular contributions by resting-state-fluctuation-of-amplitude scaling. Hum. Brain Mapp. 32, 1125–1140.10.1002/hbm.21097
    1. Liau J., Liu T. T. (2009). Inter-subject variability in hypercapnic normalization of the BOLD fMRI response. Neuroimage 45, 420–430.10.1016/j.neuroimage.2008.11.032
    1. Liu X., Zhu X. H., Chen W. (2011). Baseline BOLD correlation predicts individuals’ stimulus-evoked BOLD responses. Neuroimage 54, 2278–2286.10.1016/j.neuroimage.2010.10.001
    1. Logothetis N. K., Murayama Y., Augath M., Steffen T., Werner J., Oeltermann A. (2009). How not to study spontaneous activity. Neuroimage 45, 1080–1089.10.1016/j.neuroimage.2009.01.010
    1. Lowe M. J., Mock B. J., Sorenson J. A. (1998). Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7, 119–132.10.1006/nimg.1997.0315
    1. Lu H., Yezhuvath U. S., Xiao G. (2010). Improving fMRI sensitivity by normalization of basal physiologic state. Hum. Brain Mapp. 31, 80–87.
    1. Lu H., Zuo Y., Gu H., Waltz J. A., Zhan W., Scholl C. A., Rea W., Yang Y., Stein E. A. (2007). Synchronized delta oscillations correlate with the resting-state functional MRI signal. Proc. Natl. Acad. Sci. U.S.A. 104, 18265–18269.10.1073/pnas.0705791104
    1. Maandag N. J., Coman D., Sanganahalli B. G., Herman P., Smith A. J., Blumenfeld H., Shulman R. G., Hyder F. (2007). Energetics of neuronal signaling and fMRI activity. Proc. Natl. Acad. Sci. U.S.A. 104, 20546–20551.10.1073/pnas.0709515104
    1. Mennes M., Kelly C., Zuo X. N., Martino A. D., Biswal B., Castellanos F. X., Milham M. P. (2010). Inter-individual differences in resting state functional connectivity predict task-induced BOLD activity. Neuroimage 50, 1690–1701.10.1016/j.neuroimage.2010.01.002
    1. Pasley B. N., Inglis B. A., 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.2006.09.015
    1. Raichle M. E., MacLeod A. M., Snyder A. Z., Powers W. J., Gusnard D. A., Shulman G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676–682.10.1073/pnas.98.2.676
    1. Roy A. K., Shehzad Z., Margulies D. S., Kelly A. M., Uddin L. Q., Gotimer K., Biswal B. B., Castellanos F. X., Milham M. P. (2009). Functional connectivity of the human amygdala using resting state fMRI. Neuroimage 45, 614–626.10.1016/j.neuroimage.2008.11.030
    1. Sanganahalli B. G., Herman P., Blumenfeld H., Hyder F. (2009). Oxidative neuroenergetics in event-related paradigms. J. Neurosci. 29, 1707–1718.10.1523/JNEUROSCI.5549-08.2009
    1. Schölvinck M. L., Maier A., Ye F. Q., Duyn J. H., Leopold D. A. (2010). Neural basis of global resting-state fMRI activity. Proc. Natl. Acad. Sci. U.S.A. 107, 10238–10243.10.1073/pnas.0913110107
    1. Shmuel A., Leopold D. A. (2008). Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: implications for functional connectivity at rest. Hum. Brain Mapp. 29, 751–761.10.1002/hbm.20580
    1. Talairach J., Tournoux P. (1998). Co-planar Stereotaxic Atlas of the Human Brain. New York: Theime Medical.
    1. Thomason M. E., Glover G. H. (2008). Controlled inspiration depth reduces variance in breath-holding-induced BOLD signal. Neuroimage 39, 206–214.10.1016/j.neuroimage.2007.08.014
    1. Wise R. G., Ide K., Poulin M. J., Tracey I. (2004). Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 16, 52–64.
    1. Zang Y. F., He Y., Zhu C. Z., Cao Q. J., Sui M. Q., Liang M., Tian L. X., Jiang T. Z., Wang Y. F. (2007). Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 29, 83–91.10.1016/j.braindev.2006.07.002
    1. Zou Q. H., Zhu C. Z., Yang Y., Zuo X. N., Long X. Y., Cao Q. J., Wang Y. F., Zang Y. F. (2008). An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J. Neurosci. Methods 172, 137–141.10.1016/j.jneumeth.2008.04.012

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