Skip to main content
SpringerLink
Log in

Increased spatial granularity of left brain activation and unique age/gender signatures: a 4D frequency domain approach to cerebral lateralization at rest

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Cerebral lateralization is a well-studied topic. However, most of the research to date in functional magnetic resonance imaging (fMRI) has been carried out on hemodynamic fluctuations of voxels, networks, or regions of interest (ROIs). For example, cerebral differences can be revealed by comparing the temporal activation of an ROI in one hemisphere with the corresponding homotopic region in the other hemisphere. While this approach can reveal significant information about cerebral organization, it does not provide information about the full spatiotemporal organization of the hemispheres. The cerebral differences revealed in literature suggest that hemispheres have different spatiotemporal organization in the resting state. In this study, we evaluate cerebral lateralization in the 4D spatiotemporal frequency domain to compare the hemispheres in the context of general activation patterns at different spatial and temporal scales. We use a gender-balanced resting fMRI dataset comprising over 600 healthy subjects ranging in age from 12 to 71, that have previously been studied with a network specific voxel-wise and global analysis of lateralization (Agcaoglu, et al. NeuroImage, 2014). Our analysis elucidates significant differences in the spatiotemporal organization of brain activity between hemispheres, and generally more spatiotemporal fluctuation in the left hemisphere especially in the high spatial frequency bands, and more power in the right hemisphere in the low and middle spatial frequencies. Importantly, the identified effects are not visible in the context of a typical assessment of voxelwise, regional, or even global laterality, thus our study highlights the value of 4D spatiotemporal frequency domain analyses as a complementary and powerful tool for studying brain function.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agcaoglu, O., Miller, R., Mayer, A. R., Hugdahl, K., & Calhoun, V. D. (2014). Lateralization of resting state networks and relationship to age and gender. NeuroImage. doi:10.1016/j.neuroimage.2014.09.001.

    PubMed  PubMed Central  Google Scholar 

  • Allen, E. A., Erhardt, E. B., Damaraju, E., Gruner, W., Segall, J. M., Silva, R. F., & Calhoun, V. D. (2011). A baseline for the multivariate comparison of resting-state networks. Frontiers in Systems Neuroscience, 5, 2. doi:10.3389/fnsys.2011.00002.

    PubMed  PubMed Central  Google Scholar 

  • Baria, A. T., Baliki, M. N., Parrish, T., & Apkarian, A. V. (2011). Anatomical and functional assemblies of brain BOLD oscillations. Journal of Neuroscience, 31(21), 7910–7919. doi:10.1523/JNEUROSCI.1296-11.2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breier, J. I., Simos, P. G., Zouridakis, G., & Papanicolaou, A. C. (1999). Lateralization of cerebral activation in auditory verbal and non-verbal memory tasks using magnetoencephalography. Brain Topography, 12(2), 89–97.

    Article  CAS  PubMed  Google Scholar 

  • Broca, P. (1861). Sur le principe des localisations cerebrales. Bulletin de la Societe d’Anthropologie, 2, 190–204.

  • Cai, Q., Van der Haegen, L., & Brysbaert, M. (2013). Complementary hemispheric specialization for language production and visuospatial attention. Proceedings of the National Academy of Sciences of the United States of America, 110(4), E322–330. doi:10.1073/pnas.1212956110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calhoun, V. D., Sui, J., Kiehl, K., Turner, J., Allen, E., & Pearlson, G. (2011). Exploring the psychosis functional connectome: aberrant intrinsic networks in schizophrenia and bipolar disorder. Front Psychiatry, 2, 75. doi:10.3389/fpsyt.2011.00075.

    PubMed  Google Scholar 

  • Clements, A. M., Rimrodt, S. L., Abel, J. R., Blankner, J. G., Mostofsky, S. H., Pekar, J. J., & Cutting, L. E. (2006). Sex differences in cerebral laterality of language and visuospatial processing. Brain and Language, 98(2), 150–158. doi:10.1016/j.bandl.2006.04.007.

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove, K. P., Mazure, C. M., & Staley, J. K. (2007). Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological Psychiatry, 62(8), 847–855. doi:10.1016/j.biopsych.2007.03.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deary, I. J., Corley, J., Gow, A. J., Harris, S. E., Houlihan, L. M., Marioni, R. E., & Starr, J. M. (2009). Age-associated cognitive decline. British Medical Bulletin, 92, 135–152. doi:10.1093/bmb/ldp033.

    Article  PubMed  Google Scholar 

  • Filippi, M., Valsasina, P., Misci, P., Falini, A., Comi, G., & Rocca, M. A. (2013). The organization of intrinsic brain activity differs between genders: a resting-state fMRI study in a large cohort of young healthy subjects. Human Brain Mapping, 34(6), 1330–1343. doi:10.1002/hbm.21514.

    Article  PubMed  Google Scholar 

  • Freire, L., Roche, A., & Mangin, J. F. (2002). What is the best similarity measure for motion correction in fMRI time series? IEEE Transactions on Medical Imaging, 21(5), 470–484. doi:10.1109/TMI.2002.1009383.

    Article  CAS  PubMed  Google Scholar 

  • Garrity, A. G., Pearlson, G. D., McKiernan, K., Lloyd, D., Kiehl, K. A., & Calhoun, V. D. (2007). Aberrant “default mode” functional connectivity in schizophrenia. The American Journal of Psychiatry, 164(3), 450–457. doi:10.1176/appi.ajp.164.3.450.

    Article  PubMed  Google Scholar 

  • Genovese, C. R., Lazar, N. A., & Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage, 15(4), 870–878. doi:10.1006/nimg.2001.1037.

    Article  PubMed  Google Scholar 

  • Gobbele, R., Lamberty, K., Stephan, K. E., Stegelmeyer, U., Buchner, H., Marshall, J. C., & Waberski, T. D. (2008). Temporal activation patterns of lateralized cognitive and task control processes in the human brain. Brain Research, 1205, 81–90. doi:10.1016/j.brainres.2008.02.031.

    Article  CAS  PubMed  Google Scholar 

  • Gotts, S. J., Jo, H. J., Wallace, G. L., Saad, Z. S., Cox, R. W., & Martin, A. (2013). Two distinct forms of functional lateralization in the human brain. Proceedings of the National Academy of Sciences of the United States of America, 110(36), E3435–3444. doi:10.1073/pnas.1302581110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groen, M. A., Whitehouse, A. J., Badcock, N. A., & Bishop, D. V. (2012). Does cerebral lateralization develop? A study using functional transcranial Doppler ultrasound assessing lateralization for language production and visuospatial memory. Brain Behavior, 2(3), 256–269. doi:10.1002/brb3.56.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hellige, J. B., Laeng, B., & Michimata, C. (2010). Processing asymmetries in the visual system. In K. Hugdahl (Ed.), The Two Halves of the Brain (pp. 379–416). Cambridge: MIT Press.

    Chapter  Google Scholar 

  • Hong, X., Sun, J., Bengson, J. J., & Tong, S. (2014). Age-related spatiotemporal reorganization during response inhibition. International Journal of Psychophysiology, 93(3), 371–380. doi:10.1016/j.ijpsycho.2014.05.013.

    Article  PubMed  Google Scholar 

  • Hoptman, M. J., Zuo, X. N., Butler, P. D., Javitt, D. C., D’Angelo, D., Mauro, C. J., & Milham, M. P. (2010). Amplitude of low-frequency oscillations in schizophrenia: a resting state fMRI study. Schizophrenia Research, 117(1), 13–20. doi:10.1016/j.schres.2009.09.030.

    Article  PubMed  Google Scholar 

  • Hugdahl, K. (2011). Hemispheric asymmetry: contributions from brain imaging. Wiley Interdisciplinary Reviews: Cognitive Science, 2(5), 461–478. doi:10.1002/wcs.122.

    PubMed  Google Scholar 

  • Hugdahl, K., & Westerhausen, R. (2009). What is left is right: how speech asymmetry shaped the brain. European Psychologist, 14(1), 78–89. doi:10.1027/1016-9040.14.1.78.

    Article  Google Scholar 

  • Hugdahl, K., & Westerhausen, R. (2010). The two halves of the brain : information processing in the cerebral hemispheres. Cambridge: MIT Press.

    Book  Google Scholar 

  • Kochunov, P., Mangin, J. F., Coyle, T., Lancaster, J., Thompson, P., Riviere, D., & Fox, P. T. (2005). Age-related morphology trends of cortical sulci. Human Brain Mapping, 26(3), 210–220. doi:10.1002/hbm.20198.

    Article  PubMed  Google Scholar 

  • Liu, H., Stufflebeam, S. M., Sepulcre, J., Hedden, T., & Buckner, R. L. (2009). Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors. Proceedings of the National Academy of Sciences of the United States of America, 106(48), 20499–20503. doi:10.1073/pnas.0908073106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mather, M., & Nga, L. (2013). Age differences in thalamic low-frequency fluctuations. Neuroreport, 24(7), 349–353. doi:10.1097/WNR.0b013e32835f6784.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mazoyer, B., Zago, L., Jobard, G., Crivello, F., Joliot, M., Perchey, G., & Tzourio-Mazoyer, N. (2014). Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS One, 9(6), e101165. doi:10.1371/journal.pone.0101165.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller, R. L., Erhardt, E. B., Allen, E. A., Michael, A. M., Turner, J. A., Bustillo, J., Calhoun, V. D. (2015). Multidimensional frequency domain analysis of full-volume fMRI reveals significant effects of age, gender and mental illness on the spatiotemporal organization of resting-state brain activity. Front Neurosci, 9. doi: 10.3389/fnins.2015.00203.

  • Nielsen, J. A., Zielinski, B. A., Ferguson, M. A., Lainhart, J. E., & Anderson, J. S. (2013). An evaluation of the left-brain vs. right-brain hypothesis with resting state functional connectivity magnetic resonance imaging. PLoS One, 8(8), e71275. doi: 10.1371/journal.pone.0071275.

  • Plessen, K. J., Hugdahl, K., Bansal, R., Hao, X., & Peterson, B. S. (2014). Sex, age, and cognitive correlates of asymmetries in thickness of the cortical mantle across the life span. Journal of Neuroscience, 34(18), 6294–6302. doi:10.1523/JNEUROSCI.3692-13.2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott, A., Courtney, W., Wood, D., de la Garza, R., Lane, S., King, M., & Calhoun, V. D. (2011). COINS: an innovative informatics and neuroimaging tool suite built for large heterogeneous datasets. Front Neuroinformation, 5, 33. doi:10.3389/fninf.2011.00033.

    Google Scholar 

  • Smith, E. E., Jonides, J., & Koeppe, R. A. (1996). Dissociating verbal and spatial working memory using PET. Cerebral Cortex, 6(1), 11–20.

    Article  CAS  PubMed  Google Scholar 

  • Sperry, R. W. (1974). Lateral specialization in the surgically separated hemispheres. The Neuroscience: Third Study Program Cambridge: MIT Press., 5–19.

  • Stephan, K. E., Marshall, J. C., Friston, K. J., Rowe, J. B., Ritzl, A., Zilles, K., & Fink, G. R. (2003). Lateralized cognitive processes and lateralized task control in the human brain. Science, 301(5631), 384–386. doi:10.1126/science.1086025.

    Article  CAS  PubMed  Google Scholar 

  • Swanson, N., Eichele, T., Pearlson, G., Kiehl, K., Yu, Q., & Calhoun, V. D. (2011). Lateral differences in the default mode network in healthy controls and patients with schizophrenia. Human Brain Mapping, 32(4), 654–664. doi:10.1002/hbm.21055.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thomason, M. E., Race, E., Burrows, B., Whitfield-Gabrieli, S., Glover, G. H., & Gabrieli, J. D. (2009). Development of spatial and verbal working memory capacity in the human brain. Journal Cognitive Neuroscience, 21(2), 316–332. doi:10.1162/jocn.2008.21028.

    Article  Google Scholar 

  • Thompson, J. J., Blair, M. R., & Henrey, A. J. (2014). Over the hill at 24: persistent age-related cognitive-motor decline in reaction times in an ecologically valid video game task begins in early adulthood. PLoS One, 9(4), e94215. doi:10.1371/journal.pone.0094215.

    Article  PubMed  PubMed Central  Google Scholar 

  • Turner, J. A., Chen, H., Mathalon, D. H., Allen, E. A., Mayer, A. R., Abbott, C. C., & Bustillo, J. (2012). Reliability of the amplitude of low-frequency fluctuations in resting state fMRI in chronic schizophrenia. Psychiatry Research, 201(3), 253–255. doi:10.1016/j.pscychresns.2011.09.012.

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Dijk, K. R. A., Hedden, T., Venkataraman, A., Evans, K. C., Lazar, S. W., & Buckner, R. L. (2010). Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. Journal of Neurophysiology, 103(1), 297–321. doi:10.1152/jn.00783.2009.

    Article  PubMed  Google Scholar 

  • Wang, L., Shen, H., Tang, F., Zang, Y., & Hu, D. (2012). Combined structural and resting-state functional MRI analysis of sexual dimorphism in the young adult human brain: an MVPA approach. NeuroImage, 61(4), 931–940. doi:10.1016/j.neuroimage.2012.03.080.

    Article  PubMed  Google Scholar 

  • Welch, P. D. (1967). The use of fast fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Trans Audio Electroacoust, 0, 70–73.

  • Wernicke, C. (1874). Der aphasische Symptomencomplex. Eine psychologische Studie auf anatomischer Basis; Breslau, M. Crohn und Weigert.

  • Yang, H., Long, X. Y., Yang, Y., Yan, H., Zhu, C. Z., Zhou, X. P., & Gong, Q. Y. (2007). Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. NeuroImage, 36(1), 144–152. doi:10.1016/j.neuroimage.2007.01.054.

    Article  PubMed  Google Scholar 

  • Yu, Q., Sui, J., Liu, J., Plis, S. M., Kiehl, K. A., Pearlson, G., & Calhoun, V. D. (2013). Disrupted correlation between low frequency power and connectivity strength of resting state brain networks in schizophrenia. Schizophrenia Research, 143(1), 165–171. doi:10.1016/j.schres.2012.11.001.

    Article  PubMed  Google Scholar 

  • Zhang, Z., Lu, G., Zhong, Y., Tan, Q., Chen, H., Liao, W., & Liu, Y. (2010). fMRI study of mesial temporal lobe epilepsy using amplitude of low-frequency fluctuation analysis. Human Brain Mapping, 31(12), 1851–1861. doi:10.1002/hbm.20982.

    Article  PubMed  Google Scholar 

  • Zhu, L., Fan, Y., Zou, Q., Wang, J., Gao, J. H., & Niu, Z. (2014). Temporal reliability and lateralization of the resting-state language network. PLoS One, 9(1), e85880. doi:10.1371/journal.pone.0085880.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuo, X. N., Di Martino, A., Kelly, C., Shehzad, Z. E., Gee, D. G., Klein, D. F., & Milham, M. P. (2010a). The oscillating brain: complex and reliable. NeuroImage, 49(2), 1432–1445. doi:10.1016/j.neuroimage.2009.09.037.

    Article  PubMed  Google Scholar 

  • Zuo, X. N., Kelly, C., Di Martino, A., Mennes, M., Margulies, D. S., Bangaru, S., & Milham, M. P. (2010b). Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. Journal of Neuroscience, 30(45), 15034–15043. doi:10.1523/JNEUROSCI.2612-10.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported in part by NIH grants including 2R01EB005846 and a Center of Biomedical Research Excellence (COBRE) grant P20GM103472.

Author information

Authors and Affiliations

  1. Mind Research Network, 1001 Yale Blvd. NE, Albuquerque, NM, 87106, USA

    O. Agcaoglu, R. Miller, A. R. Mayer & V. D. Calhoun

  2. Department of Electrical and Computer Engineering, University of New Mexico, Albuquerque, NM, USA

    O. Agcaoglu & V. D. Calhoun

  3. University of New Mexico Health Science Center, Albuquerque, NM, USA

    A. R. Mayer

  4. Department Biological and Medical Psychology, University of Bergen, Bergen, Norway

    K. Hugdahl

Authors
  1. O. Agcaoglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. R. Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Hugdahl
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. V. D. Calhoun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. Agcaoglu.

Ethics declarations

• This study was fund in part by NIH grants including 2R01EB005846 and a Center of Biomedical Research Excellence (COBRE) grant P20GM103472.

• Author Oktay Agcaoglu, Author Robyn Miller, Author Andy Mayer, Author Kenneth Hugdahl and Author Vince D. Calhoun declare that they have no conflict of interest.

• All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Agcaoglu, O., Miller, R., Mayer, A.R. et al. Increased spatial granularity of left brain activation and unique age/gender signatures: a 4D frequency domain approach to cerebral lateralization at rest. Brain Imaging and Behavior 10, 1004–1014 (2016). https://doi.org/10.1007/s11682-015-9463-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-015-9463-8

Keywords

Search

Navigation