Hostname: page-component-848d4c4894-m9kch Total loading time: 0 Render date: 2024-05-16T16:02:04.674Z Has data issue: false hasContentIssue false
  • English
  • Français

Seasonality in regional brain glucose metabolism

Published online by Cambridge University Press:  18 April 2024

Rui Zhang Open the ORCID record for Rui Zhang [Opens in a new window] ,
Dardo Tomasi ,
Ehsan Shokri-Kojori ,
Peter Manza ,
Sukru Baris Demiral ,
Gene-Jack Wang  and
Nora D. Volkow
Rui Zhang*
Affiliation:
National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD 20892, USA
Dardo Tomasi
Affiliation:
National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD 20892, USA
Ehsan Shokri-Kojori
Affiliation:
National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD 20892, USA
Peter Manza
Affiliation:
National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD 20892, USA
Sukru Baris Demiral
Affiliation:
National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD 20892, USA
Gene-Jack Wang
Affiliation:
National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD 20892, USA
Nora D. Volkow*
Affiliation:
National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD 20892, USA
*
Corresponding author: Rui Zhang; Email: rui.zhang@nih.gov; Nora D. Volkow; Email: nvolkow@nida.nih.gov
Corresponding author: Rui Zhang; Email: rui.zhang@nih.gov; Nora D. Volkow; Email: nvolkow@nida.nih.gov
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Daylength and the rates of changes in daylength have been associated with seasonal fluctuations in psychiatric symptoms and in cognition and mood in healthy adults. However, variations in human brain glucose metabolism in concordance with seasonal changes remain under explored.

Methods

In this cross-sectional study, we examined seasonal effects on brain glucose metabolism, which we measured using 18F-fluorodeoxyglucose-PET in 97 healthy participants. To maximize the sensitivity of regional effects, we computed relative metabolic measures by normalizing the regional measures to white matter metabolism. Additionally, we explored the role of rest–activity rhythms/sleep–wake activity measured with actigraphy in the seasonal variations of regional brain metabolic activity.

Results

We found that seasonal variations of cerebral glucose metabolism differed across brain regions. Glucose metabolism in prefrontal regions increased with longer daylength and with greater day-to-day increases in daylength. The cuneus and olfactory bulb had the maximum and minimum metabolic values around the summer and winter solstice respectively (positively associated with daylength), whereas the temporal lobe, brainstem, and postcentral cortex showed maximum and minimum metabolic values around the spring and autumn equinoxes, respectively (positively associated with faster daylength gain). Longer daylength was associated with greater amplitude and robustness of diurnal activity rhythms suggesting circadian involvement.

Conclusions

The current findings advance our knowledge of seasonal patterns in a key indicator of brain function relevant for mood and cognition. These data could inform treatment interventions for psychiatric symptoms that peak at specific times of the year.

Keywords

cerebral glucose metabolismcircadian rhythmsdaylengthseasonal effects
Type
Original Article
Information
Psychological Medicine , First View , pp. 1 - 9
Check for updates
Creative Commons
This is a work of the US Government and is not subject to copyright protection within the United States. Published by Cambridge University Press
Copyright
Copyright © National Institutes of Health, 2024

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amodio, D. M., & Frith, C. D. (2006). Meeting of minds: The medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7(4), 268–277. doi: 10.1038/nrn1884CrossRefGoogle ScholarPubMed
Ancoli-Israel, S., Cole, R., Alessi, C., Chambers, M., Moorcroft, W., & Pollak, C. P. (2003). The role of actigraphy in the study of sleep and circadian rhythms. Sleep, 26(3), 342–392. doi: 10.1093/sleep/26.3.342CrossRefGoogle Scholar
Andersen, R. A., & Buneo, C. A. (2003). Sensorimotor integration in posterior parietal cortex. Advances in Neurology, 93, 159–177.Google ScholarPubMed
Bano-Otalora, B., Martial, F., Harding, C., Bechtold, D. A., Allen, A. E., Brown, T. M., … Lucas, R. J. (2021). Bright daytime light enhances circadian amplitude in a diurnal mammal. Proceedings of the National Academy of Sciences of the USA, 118(22), e2100094118. doi: 10.1073/pnas.2100094118CrossRefGoogle Scholar
Chadwick, M. J., Anjum, R. S., Kumaran, D., Schacter, D. L., Spiers, H. J., & Hassabis, D. (2016). Semantic representations in the temporal pole predict false memories. Proceedings of the National Academy of Sciences, 113(36), 10180–10185. doi: 10.1073/pnas.1610686113CrossRefGoogle ScholarPubMed
Chellappa, S. L., Ly, J. Q. M., Meyer, C., Balteau, E., Degueldre, C., Luxen, A., … Vandewalle, G. (2014). Photic memory for executive brain responses. Proceedings of the National Academy of Sciences, 111(16), 6087–6091. doi: 10.1073/pnas.1320005111CrossRefGoogle ScholarPubMed
Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., … Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980. doi: 10.1016/j.neuroimage.2006.01.021CrossRefGoogle ScholarPubMed
Dienel, G. A. (2019). Brain glucose metabolism: Integration of energetics with function. Physiological Reviews, 99(1), 949–1045. doi: 10.1152/physrev.00062.2017CrossRefGoogle ScholarPubMed
Dopico, X. C., Evangelou, M., Ferreira, R. C., Guo, H., Pekalski, M. L., Smyth, D. J., … Todd, J. A. (2015). Widespread seasonal gene expression reveals annual differences in human immunity and physiology. Nature Communications, 6, 7000. doi: 10.1038/ncomms8000CrossRefGoogle ScholarPubMed
Dotson, V. M., Bogoian, H. R., Gradone, A. M., Taiwo, Z., & Minto, L. R. (2022). Subthreshold depressive symptoms relate to cuneus structure: Thickness asymmetry and sex differences. Journal of Psychiatric Research, 145, 144–147. doi: 10.1016/j.jpsychires.2021.12.013CrossRefGoogle Scholar
du Boisgueheneuc, F., Levy, R., Volle, E., Seassau, M., Duffau, H., Kinkingnehun, S., … Dubois, B. (2006). Functions of the left superior frontal gyrus in humans: A lesion study. Brain: A Journal of Neurology, 129(Pt 12), 3315–3328. doi: 10.1093/brain/awl244CrossRefGoogle ScholarPubMed
Esaki, Y., Obayashi, K., Saeki, K., Fujita, K., Iwata, N., & Kitajima, T. (2023). Habitual light exposure and circadian activity rhythms in bipolar disorder: A cross-sectional analysis of the APPLE cohort. Journal of Affective Disorders, 323, 762–769. doi: 10.1016/j.jad.2022.12.034CrossRefGoogle ScholarPubMed
Fernandez, D. C., Fogerson, P. M., Lazzerini Ospri, L., Thomsen, M. B., Layne, R. M., Severin, D., … Hattar, S. (2018). Light affects mood and learning through distinct retina-brain pathways. Cell, 175(1), 71–84.e18. doi: 10.1016/j.cell.2018.08.004CrossRefGoogle ScholarPubMed
Foland-Ross, L. C., Cooney, R. E., Joormann, J., Henry, M. L., & Gotlib, I. H. (2014). Recalling happy memories in remitted depression: A neuroimaging investigation of the repair of sad mood. Cognitive, Affective & Behavioral Neuroscience, 14(2), 818–826. doi: 10.3758/s13415-013-0216-0CrossRefGoogle ScholarPubMed
Forni, D., Pozzoli, U., Cagliani, R., Tresoldi, C., Menozzi, G., Riva, S., … Sironi, M. (2014). Genetic adaptation of the human circadian clock to day-length latitudinal variations and relevance for affective disorders. Genome Biology, 15(10), 499. doi: 10.1186/s13059-014-0499-7CrossRefGoogle ScholarPubMed
Fu, X., Lu, Z., Wang, Y., Huang, L., Wang, X., Zhang, H., & Xiao, Z. (2017). A clinical research study of cognitive dysfunction and affective impairment after isolated brainstem stroke. Frontiers in Aging Neuroscience, 9, 400. doi: 10.3389/fnagi.2017.00400CrossRefGoogle ScholarPubMed
Germino, M., Gallezot, J.-D., Yan, J., & Carson, R. E. (2017). Direct reconstruction of parametric images for brain PET with event-by-event motion correction: Evaluation in two tracers across count levels. Physics in Medicine and Biology, 62(13), 5344–5364. doi: 10.1088/1361-6560/aa731fCrossRefGoogle ScholarPubMed
Glasser, M. F., Sotiropoulos, S. N., Wilson, J. A., Coalson, T. S., Fischl, B., Andersson, J. L., … Jenkinson, M. (2013). The minimal preprocessing pipelines for the human connectome project. NeuroImage, 80, 105–124. doi: 10.1016/j.neuroimage.2013.04.127CrossRefGoogle ScholarPubMed
Golder, S. A., & Macy, M. W. (2011). Diurnal and seasonal mood vary with work, sleep, and daylength across diverse cultures. Science, 333(6051), 1878–1881. doi: 10.1126/science.1202775CrossRefGoogle ScholarPubMed
Hastings, M. H., Maywood, E. S., & Brancaccio, M. (2018). Generation of circadian rhythms in the suprachiasmatic nucleus. Nature Reviews Neuroscience, 19(8), 453–469. doi: 10.1038/s41583-018-0026-zCrossRefGoogle ScholarPubMed
Hattar, S., Liao, H.-W., Takao, M., Berson, D. M., & Yau, K.-W. (2002). Melanopsin-containing retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity. Science, 295(5557), 1065–1070. doi: 10.1126/science.1069609CrossRefGoogle ScholarPubMed
Hofman, M. A., Purba, J. S., & Swaab, D. F. (1993). Annual variations in the vasopressin neuron population of the human suprachiasmatic nucleus. Neuroscience, 53(4), 1103–1112. doi: 10.1016/0306-4522(93)90493-YCrossRefGoogle ScholarPubMed
Hofman, M. A., & Swaab, D. F. (1993). Diurnal and seasonal rhythms of neuronal activity in the suprachiasmatic nucleus of humans. Journal of Biological Rhythms, 8(4), 283–295. doi: 10.1177/074873049300800402CrossRefGoogle ScholarPubMed
Hu, S., Ide, J. S., Zhang, S., & Li, C. R. (2016). The right superior frontal gyrus and individual variation in proactive control of impulsive response. Journal of Neuroscience, 36(50), 12688–12696. doi: 10.1523/JNEUROSCI.1175-16.2016CrossRefGoogle ScholarPubMed
Huang, S. C., Phelps, M. E., Hoffman, E. J., Sideris, K., Selin, C. J., & Kuhl, D. E. (1980). Noninvasive determination of local cerebral metabolic rate of glucose in man. The American Journal of Physiology, 238(1), E69–E82. doi: 10.1152/ajpendo.1980.238.1.E69Google ScholarPubMed
Ishibashi, K., Wagatsuma, K., Ishiwata, K., & Ishii, K. (2016). Alteration of the regional cerebral glucose metabolism in healthy subjects by glucose loading. Human Brain Mapping, 37(8), 2823–2832. doi: 10.1002/hbm.23210CrossRefGoogle ScholarPubMed
Kohno, K., Terao, T., Hatano, K., Kodama, K., Makino, M., Mizokami, Y., … Yano, T. (2016). Postcomparison of [(18) F]-fluorodeoxyglucose uptake in the brain after short-term bright light exposure and no intervention. Acta Psychiatrica Scandinavica, 134(1), 65–72. doi: 10.1111/acps.12569CrossRefGoogle ScholarPubMed
LaDage, L. D. (2022). Seasonal variation in gonadal hormones, spatial cognition, and hippocampal attributes: More questions than answers. Hormones and Behavior, 141, 105151. doi: 10.1016/j.yhbeh.2022.105151CrossRefGoogle ScholarPubMed
LeGates, T. A., Altimus, C. M., Wang, H., Lee, H.-K., Yang, S., Zhao, H., … Hattar, S. (2012). Aberrant light directly impairs mood and learning through melanopsin-expressing neurons. Nature, 491(7425), 594–598. doi: 10.1038/nature11673CrossRefGoogle ScholarPubMed
Marler, M. R., Gehrman, P., Martin, J. L., & Ancoli-Israel, S. (2006). The sigmoidally transformed cosine curve: A mathematical model for circadian rhythms with symmetric non-sinusoidal shapes. Statistics in Medicine, 25(22), 3893–3904. doi: 10.1002/sim.2466CrossRefGoogle ScholarPubMed
Meijer, J. H., Michel, S., Vanderleest, H. T., & Rohling, J. H. T. (2010). Daily and seasonal adaptation of the circadian clock requires plasticity of the SCN neuronal network. The European Journal of Neuroscience, 32(12), 2143–2151. doi: 10.1111/j.1460-9568.2010.07522.xCrossRefGoogle ScholarPubMed
Meyer, C., Muto, V., Jaspar, M., Kussé, C., Lambot, E., Chellappa, S. L., … Vandewalle, G. (2016). Seasonality in human cognitive brain responses. Proceedings of the National Academy of Sciences, 113(11), 3066–3071. doi: 10.1073/pnas.1518129113CrossRefGoogle ScholarPubMed
Mouly, A.-M., & Sullivan, R. (2010). Memory and plasticity in the olfactory system: From infancy to adulthood. In Menini, A. (Ed.), The neurobiology of olfaction. Boca Raton, FL: CRC Press/Taylor & Francis. Retrieved from https://www.ncbi.nlm.nih.gov/books/NBK55967/.Google Scholar
Olson, I. R., Plotzker, A., & Ezzyat, Y. (2007). The enigmatic temporal pole: A review of findings on social and emotional processing. Brain, 130(7), 1718–1731. doi: 10.1093/brain/awm052CrossRefGoogle Scholar
Perrin, F., Peigneux, P., Fuchs, S., Verhaeghe, S., Laureys, S., Middleton, B., … Dijk, D.-J. (2004). Nonvisual responses to light exposure in the human brain during the circadian night. Current Biology, 14(20), 1842–1846. doi: 10.1016/j.cub.2004.09.082CrossRefGoogle ScholarPubMed
Phelps, M. E., Huang, S. C., Hoffman, E. J., Selin, C., Sokoloff, L., & Kuhl, D. E. (1979). Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: Validation of method. Annals of Neurology, 6(5), 371–388. doi: 10.1002/ana.410060502CrossRefGoogle ScholarPubMed
Polich, J., & Geisler, M. W. (1991). P300 seasonal variation. Biological Psychology, 32(2–3), 173–179. doi: 10.1016/0301-0511(91)90008-5CrossRefGoogle ScholarPubMed
Ripp, I., Wallenwein, L. A., Wu, Q., Emch, M., Koch, K., Cumming, P., & Yakushev, I. (2021). Working memory task induced neural activation: A simultaneous PET/fMRI study. NeuroImage, 237, 118131. doi: 10.1016/j.neuroimage.2021.118131CrossRefGoogle ScholarPubMed
Skeldon, A. C., Dijk, D.-J., Meyer, N., & Wulff, K. (2022). Extracting circadian and sleep parameters from longitudinal data in schizophrenia for the design of pragmatic light interventions. Schizophrenia Bulletin, 48(2), 447–456. doi: 10.1093/schbul/sbab124CrossRefGoogle ScholarPubMed
Soudry, Y., Lemogne, C., Malinvaud, D., Consoli, S.-M., & Bonfils, P. (2011). Olfactory system and emotion: Common substrates. European Annals of Otorhinolaryngology, Head and Neck Diseases, 128(1), 18–23. doi: 10.1016/j.anorl.2010.09.007CrossRefGoogle ScholarPubMed
van Hees, V. T., Fang, Z., Langford, J., Assah, F., Mohammad, A., da Silva, I. C. M., … Brage, S. (2014). Autocalibration of accelerometer data for free-living physical activity assessment using local gravity and temperature: An evaluation on four continents. Journal of Applied Physiology, 117(7), 738–744. doi: 10.1152/japplphysiol.00421.2014CrossRefGoogle ScholarPubMed
van Hees, V. T., Sabia, S., Anderson, K. N., Denton, S. J., Oliver, J., Catt, M., … Singh-Manoux, A. (2015). A novel, open access method to assess sleep duration using a wrist-worn accelerometer. PLoS ONE, 10(11), e0142533. doi: 10.1371/journal.pone.0142533CrossRefGoogle ScholarPubMed
van Someren, E. J. W., Hagebeuk, E. E. O., Lijzenga, C., Scheltens, P., de Rooij, S. E. J. A., Jonker, C., … Swaab, D. F. (1996). Circadian rest-activity rhythm disturbances in Alzheimer's disease. Biological Psychiatry, 40(4), 259–270. doi: 10.1016/0006-3223(95)00370-3CrossRefGoogle ScholarPubMed
Vandewalle, G., Balteau, E., Phillips, C., Degueldre, C., Moreau, V., Sterpenich, V., … Maquet, P. (2006). Daytime light exposure dynamically enhances brain responses. Current Biology, 16(16), 1616–1621. doi: 10.1016/j.cub.2006.06.031CrossRefGoogle ScholarPubMed
Vandewalle, G., Gais, S., Schabus, M., Balteau, E., Carrier, J., Darsaud, A., … Maquet, P. (2007a). Wavelength-dependent modulation of brain responses to a working memory task by daytime light exposure. Cerebral Cortex, 17(12), 2788–2795. doi: 10.1093/cercor/bhm007CrossRefGoogle ScholarPubMed
Vandewalle, G., Maquet, P., & Dijk, D.-J. (2009). Light as a modulator of cognitive brain function. Trends in Cognitive Sciences, 13(10), 429–438. doi: 10.1016/j.tics.2009.07.004CrossRefGoogle ScholarPubMed
Vandewalle, G., Schmidt, C., Albouy, G., Sterpenich, V., Darsaud, A., Rauchs, G., … Dijk, D.-J. (2007b). Brain responses to violet, blue, and green monochromatic light exposures in humans: Prominent role of blue light and the brainstem. PLoS ONE, 2(11), e1247. doi: 10.1371/journal.pone.0001247CrossRefGoogle ScholarPubMed
Vandewalle, G., Schwartz, S., Grandjean, D., Wuillaume, C., Balteau, E., Degueldre, C., … Maquet, P. (2010). Spectral quality of light modulates emotional brain responses in humans. Proceedings of the National Academy of Sciences of the USA, 107(45), 19549–19554. doi: 10.1073/pnas.1010180107CrossRefGoogle ScholarPubMed
Vanni, S., Tanskanen, T., Seppä, M., Uutela, K., & Hari, R. (2001). Coinciding early activation of the human primary visual cortex and anteromedial cuneus. Proceedings of the National Academy of Sciences of the USA, 98(5), 2776–2780. doi: 10.1073/pnas.041600898CrossRefGoogle ScholarPubMed
Wang, C., Zhang, Z., Che, L., Wu, Y., Qian, H., & Guo, X. (2021). The gray matter volume in superior frontal gyrus mediates the impact of reflection on emotion in internet gaming addicts. Psychiatry Research: Neuroimaging, 310, 111269. doi: 10.1016/j.pscychresns.2021.111269CrossRefGoogle ScholarPubMed
Wang, G. J., Volkow, N. D., Wolf, A. P., Brodie, J. D., & Hitzemann, R. J. (1994). Intersubject variability of brain glucose metabolic measurements in young normal males. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine, 35(9), 1457–1466.Google ScholarPubMed
Waugh, C. E., Lemus, M. G., & Gotlib, I. H. (2014). The role of the medial frontal cortex in the maintenance of emotional states. Social Cognitive and Affective Neuroscience, 9(12), 2001–2009. doi: 10.1093/scan/nsu011CrossRefGoogle ScholarPubMed
Wehr, T. A. (1998). Effect of seasonal changes in daylength on human neuroendocrine function. Hormone Research in Paediatrics, 49(3–4), 118–124. doi: 10.1159/000023157CrossRefGoogle ScholarPubMed
Wucher, V., Sodaei, R., Amador, R., Irimia, M., & Guigó, R. (2023). Day-night and seasonal variation of human gene expression across tissues. PLoS Biology, 21(2), e3001986. doi: 10.1371/journal.pbio.3001986CrossRefGoogle ScholarPubMed
Yang, Z., Cummings, J. L., Kinney, J. W., & Cordes, D., & Alzheimer's Disease Neuroimaging Initiative. (2023). Accelerated hypometabolism with disease progression associated with faster cognitive decline among amyloid positive patients. Frontiers in Neuroscience, 17, 1151820. doi: 10.3389/fnins.2023.1151820CrossRefGoogle ScholarPubMed
Zhang, R., Shokri-Kojori, E., & Volkow, N. D. (2023). Seasonal effect – An overlooked factor in neuroimaging research. Translational Psychiatry, 13(1), 1–6. doi: 10.1038/s41398-023-02530-2CrossRefGoogle ScholarPubMed
Zhang, R., & Volkow, N. D. (2023). Seasonality of brain function: Role in psychiatric disorders. Translational Psychiatry, 13(1), 1–11. doi: 10.1038/s41398-023-02365-xCrossRefGoogle ScholarPubMed
Supplementary material: File

Zhang et al. supplementary material

Zhang et al. supplementary material
Download Zhang et al. supplementary material(File)
File 15 KB