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Neuroradiology

, Volume 61, Issue 5, pp 575–584 | Cite as

Altered coupling of spontaneous brain activities and brain temperature in patients with adolescent-onset, first-episode, drug-naïve schizophrenia

  • Zhiyong Zhao
  • Guojun Xu
  • Bin Sun
  • Xuzhou Li
  • Zhe Shen
  • Shangda Li
  • Yi Xu
  • Manli Huang
  • Dongrong XuEmail author
Functional Neuroradiology

Abstract

Purpose

A recent study has reported that schizophrenia patients show an uncoupled association between intraventricular brain temperature (BT) and cerebral blood flow (CBF). CBF has been found to be closely coupled with spontaneous brain activities (SBAs) derived from resting-state BOLD fMRI metrics. Yet, it is unclear so far whether the relationship between the intraventricular BT and the SBAs may change in patients with adolescent-onset schizophrenia (AOS) compared with that in healthy controls (HCs).

Methods

The present study recruited 28 first-episode, drug-naïve AOS patients and 22 matched HCs. We measured the temperature of the lateral ventricles (LV) using diffusion-weighted imaging thermometry and measured SBAs using both regional homogeneity and amplitude of low-frequency fluctuation methods. A nonparametric Wilcoxon rank sum test was used to detect the difference in intraventricular BT between AOS patients and HCs with LV volume, age, and sex as covariates. We also evaluated the relationship between the intraventricular BT and the SBAs using partial correlation analysis controlling for LV volume, age, and sex.

Results

We found that HCs showed a significant negative correlation between the intraventricular BT and the local SBAs in the bilateral putamina and left superior temporal gyrus, while such a correlation was absent in AOS patients. Additionally, no significant difference between the two groups was found in the intraventricular BT.

Conclusion

These findings suggest that AOS patients may experience an uncoupling between intraventricular BT and SBAs in several schizophrenia-related brain areas, which may be associated with the altered relationships among intraventricular BT, CBF, and metabolism.

Keywords

Spontaneous brain activities Intraventricular brain temperature Adolescent-onset schizophrenia Diffusion-weighted imaging thermometry Resting-state fMRI 

Notes

Acknowledgements

The authors thank Dr. Michael Grunebaum, Columbia University, for his valuable help in writing this manuscript and his comments on clinical interpretations of this work.

Funding

This study was funded in part by the China National Key R&D Program (No. 2017YFC1308500/2017YFC1308502 & No. 2016YFC1307005), the China National Science Foundation (No.81471734), the Basic Public Welfare Research Projects in Zhejiang Province (No. LGF18H090003) and the Major Subject of Zhejiang Province (No. 2015C03054).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants (or their parents/legal guardians) included in the study.

Supplementary material

234_2019_2181_MOESM1_ESM.pdf (612 kb)
ESM 1 (PDF 611 kb)

References

  1. 1.
    Sekar A, Bialas AR, de Rivera H, Davis A, Hammond TR, Kamitaki N, Tooley K, Presumey J, Baum M, Van Doren V (2016) Schizophrenia risk from complex variation of complement component 4. Nature 530(7589):177–183Google Scholar
  2. 2.
    Shiloh R, Kushnir T, Gilat Y, Gross-Isseroff R, Hermesh H, Munitz H, Stryjer R, Weizman A, Manor D (2008) In vivo occipital–frontal temperature-gradient in schizophrenia patients and its possible association with psychopathology: a magnetic resonance spectroscopy study. Eur Neuropsychopharmacol 18(8):557–564Google Scholar
  3. 3.
    Chong TW, Castle DJ (2004) Layer upon layer: thermoregulation in schizophrenia. Schizophr Res 69(2):149–157Google Scholar
  4. 4.
    Shiloh R, Portuguese S, Bodinger L, Katz N, Sigler M, Hermesh H, Munitz H, Weizman A (2003) Increased corneal temperature in drug-free male schizophrenia patients. Eur Neuropsychopharmacol 13(1):49–52Google Scholar
  5. 5.
    Shiloh R, Weizman A, Epstein Y, Rosenberg S-L, Valevski A, Dorfman-Etrog P, Wiezer N, Katz N, Munitz H, Hermesh H (2001) Abnormal thermoregulation in drug-free male schizophrenia patients. Eur Neuropsychopharmacol 11(4):285–288Google Scholar
  6. 6.
    Posporelis S, Coughlin JM, Marsman A, Pradhan S, Tanaka T, Wang H, Varvaris M, Ward R, Higgs C, Edwards JA (2017) Decoupling of brain temperature and glutamate in recent onset of schizophrenia: a 7T proton magnetic resonance spectroscopy study. In: Biological Psychiatry: Cognitive Neuroscience and NeuroimagingGoogle Scholar
  7. 7.
    Nybo L, Secher NH, Nielsen B (2002) Inadequate heat release from the human brain during prolonged exercise with hyperthermia. J Physiol 545(2):697–704Google Scholar
  8. 8.
    Ota M, Sato N, Sakai K, Okazaki M, Maikusa N, Hattori K, Hori H, Teraishi T, Shimoji K, Yamada K (2014) Altered coupling of regional cerebral blood flow and brain temperature in schizophrenia compared with bipolar disorder and healthy subjects. J Cereb Blood Flow Metab 34(12):1868–1872Google Scholar
  9. 9.
    Hill K, Mann L, Laws K, Stephenson C, Nimmo-Smith I, McKenna P (2004) Hypofrontality in schizophrenia: a meta-analysis of functional imaging studies. Acta Psychiatr Scand 110(4):243–256Google Scholar
  10. 10.
    Jensen JE, Miller J, Williamson PC, Neufeld RW, Menon RS, Malla A, Manchanda R, Schaefer B, Densmore M, Drost DJ (2006) Grey and white matter differences in brain energy metabolism in first episode schizophrenia: 31P-MRS chemical shift imaging at 4 Tesla. Psychiatry Res Neuroimaging 146(2):127–135Google Scholar
  11. 11.
    Smesny S, Rosburg T, Nenadic I, Fenk KP, Kunstmann S, Rzanny R, Volz H-P, Sauer H (2007) Metabolic mapping using 2D 31P-MR spectroscopy reveals frontal and thalamic metabolic abnormalities in schizophrenia. NeuroImage 35(2):729–737Google Scholar
  12. 12.
    Walther S, Federspiel A, Horn H, Razavi N, Wiest R, Dierks T, Strik W, Müller TJ (2011) Resting state cerebral blood flow and objective motor activity reveal basal ganglia dysfunction in schizophrenia. Psychiatry Res Neuroimaging 192(2):117–124Google Scholar
  13. 13.
    Kindler J, Jann K, Homan P, Hauf M, Walther S, Strik W, Dierks T, Hubl D (2013) Static and dynamic characteristics of cerebral blood flow during the resting state in schizophrenia. Schizophrenia bulletin 41(1):163–170Google Scholar
  14. 14.
    Zhu J, Zhuo C, Qin W, Xu Y, Xu L, Liu X, Yu C (2015) Altered resting-state cerebral blood flow and its connectivity in schizophrenia. J Psychiatr Res 63:28–35Google Scholar
  15. 15.
    Ben-Shachar D, Bonne O, Chisin R, Klein E, Lester H, Aharon-Peretz J, Yona I, Freedman N (2007) Cerebral glucose utilization and platelet mitochondrial complex I activity in schizophrenia: a FDG-PET study. Prog Neuro-Psychopharmacol Biol Psychiatry 31(4):807–813Google Scholar
  16. 16.
    Yang J, Chen T, Sun L, Zhao Z, Qi X, Zhou K, Cao Y, Wang X, Qiu Y, Su M (2013) Potential metabolite markers of schizophrenia. Mol Psychiatry 18(1):67Google Scholar
  17. 17.
    Prabakaran S, Swatton J, Ryan M, Huffaker S, Huang J-J, Griffin J, Wayland M, Freeman T, Dudbridge F, Lilley K (2004) Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 9(7):684Google Scholar
  18. 18.
    Zhang J, Chu K, Hazlett E, Buchsbaum M (2013) A FDG-PET and fMRI study on glucose metabolism and hemodynamic response during visual attentional performance in schizophrenia. OMICS J Radiology 2(149):2Google Scholar
  19. 19.
    Aiello M, Salvatore E, Cachia A, Pappatà S, Cavaliere C, Prinster A, Nicolai E, Salvatore M, Baron J-C, Quarantelli M (2015) Relationship between simultaneously acquired resting-state regional cerebral glucose metabolism and functional MRI: a PET/MR hybrid scanner study. NeuroImage 113:111–121Google Scholar
  20. 20.
    Jann K, Gee DG, Kilroy E, Schwab S, Smith RX, Cannon TD, Wang DJ (2015) Functional connectivity in BOLD and CBF data: similarity and reliability of resting brain networks. NeuroImage 106:111–122Google Scholar
  21. 21.
    Li Z, Zhu Y, Childress AR, Detre JA, Wang Z (2012) Relations between BOLD fMRI-derived resting brain activity and cerebral blood flow. PLoS One 7(9):e44556Google Scholar
  22. 22.
    Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. NeuroImage 22(1):394–400Google Scholar
  23. 23.
    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(2):83–91Google Scholar
  24. 24.
    Alonso-Solís A, Vives-Gilabert Y, Portella MJ, Rabella M, Grasa EM, Roldán A, Keymer-Gausset A, Molins C, Núñez-Marín F, Gómez-Ansón B (2017) Altered amplitude of low frequency fluctuations in schizophrenia patients with persistent auditory verbal hallucinations. Schizophr Res 189:97–103Google Scholar
  25. 25.
    Zhuo C-J, Zhu J-J, Wang C-L, Wang L-N, Li J, Qin W (2016) Increased local spontaneous neural activity in the left precuneus specific to auditory verbal hallucinations of schizophrenia. Chin Med J 129(7):809Google Scholar
  26. 26.
    Cui L-B, Liu K, Li C, Wang L-X, Guo F, Tian P, Wu Y-J, Guo L, Liu W-M, Xi Y-B (2016) Putamen-related regional and network functional deficits in first-episode schizophrenia with auditory verbal hallucinations. Schizophr Res 173(1):13–22Google Scholar
  27. 27.
    Wagner MW, Stern SE, Oshmyansky A, Huisman TA, Poretti A (2016) The role of ADC-based thermometry in measuring brain intraventricular temperature in children. J Neuroimaging 26(3):315–323Google Scholar
  28. 28.
    Sakai K, Yamada K, Mori S, Sugimoto N, Nishimura T (2011) Age-dependent brain temperature decline assessed by diffusion-weighted imaging thermometry. NMR Biomed 24(9):1063–1067Google Scholar
  29. 29.
    Egashira K, Matsuo K, Mihara T, Nakano M, Nakashima M, Watanuki T, Matsubara T, Watanabe Y (2014) Different and shared brain volume abnormalities in late-and early-onset schizophrenia. Neuropsychobiology 70(3):142–151Google Scholar
  30. 30.
    Van Assche L, Morrens M, Luyten P, Van de Ven L, Vandenbulcke M (2017) The neuropsychology and neurobiology of late-onset schizophrenia and very-late-onset schizophrenia-like psychosis: a critical review. Neurosci Biobehav Rev 83:604–621Google Scholar
  31. 31.
    Kozak L, Bango M, Szabo M, Rudas G, Vidnyanszky Z, Nagy Z (2010) Using diffusion MRI for measuring the temperature of cerebrospinal fluid within the lateral ventricles. Acta Paediatr 99(2):237–243Google Scholar
  32. 32.
    Sone D, Ota M, Yokoyama K, Sumida K, Kimura Y, Imabayashi E, Matsuda H, Sato N (2016) Noninvasive evaluation of the correlation between regional cerebral blood flow and intraventricular brain temperature in temporal lobe epilepsy. Magn Reson Imaging 34(4):451–454Google Scholar
  33. 33.
    Wang S, Zhan Y, Zhang Y, Lv L, Wu R, Zhao J, Guo W (2017) Abnormal functional connectivity strength in patients with adolescent-onset schizophrenia: a resting-state fMRI study. Eur Child Adolesc Psychiatry 26(7):839–845Google Scholar
  34. 34.
    Kay SR, Flszbein A, Opfer LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13(2):261Google Scholar
  35. 35.
    Andersson JLR, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. NeuroImage 125:1063–1078.  https://doi.org/10.1016/j.neuroimage.2015.10.019 Google Scholar
  36. 36.
    Zhao Z, Huang T, Tang C, Ni K, Pan X, Yan C, Fan X, Xu D, Luo Y (2017) Altered resting-state intra-and inter-network functional connectivity in patients with persistent somatoform pain disorder. PLoS One 12(4):e0176494Google Scholar
  37. 37.
    Zhao Z, Tang C, Yin D, Wu J, Gong J, Sun L, Jia J, Xu D, Fan M (2018) Frequency-specific alterations of regional homogeneity in subcortical stroke patients with different outcomes in hand function. Hum Brain Mapp 39(11):4373–4384Google Scholar
  38. 38.
    Mills R (1973) Self-diffusion in normal and heavy water in the range 1-45. Deg. J Phys Chem 77(5):685–688Google Scholar
  39. 39.
    Sakai K, Yamada K, Sugimoto N (2012) Calculation methods for ventricular diffusion-weighted imaging thermometry: phantom and volunteer studies. NMR Biomed 25(2):340–346Google Scholar
  40. 40.
    Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289Google Scholar
  41. 41.
    Price CJ (2010) The anatomy of language: a review of 100 fMRI studies published in 2009. Ann N Y Acad Sci 1191(1):62–88Google Scholar
  42. 42.
    Obeso JA, Rodriguez-Oroz MC, Stamelou M, Bhatia KP, Burn DJ (2014) The expanding universe of disorders of the basal ganglia. Lancet 384(9942):523–531Google Scholar
  43. 43.
    Li Z, Lei W, Deng W, Zheng Z, Li M, Max X, Wang Q, Huang C, Li N, Collier DA (2017) Aberrant spontaneous neural activity and correlation with evoked-brain potentials in first-episode, treatment-naïve patients with deficit and non-deficit schizophrenia. Psychiatry Res Neuroimaging 261:9–19Google Scholar
  44. 44.
    Turner JA, Damaraju E, Van Erp TGM, Mathalon DH, Ford JM, Voyvodic J, Mueller BA, Belger A, Bustillo J, McEwen S, Olkin SG, FBIRN, Calhoun VD (2013) A multi-site resting state fMRI study on the amplitude of low frequency fluctuations in schizophrenia. Front Neurosci 7(7):137Google Scholar
  45. 45.
    Listed N (2010) Regional cerebral blood flow in first-episode schizophrenia patients before and after antipsychotic drug treatment. Scottish Schizophrenia Research Group. Acta Psychiatr Scand 97(6):440–449Google Scholar
  46. 46.
    Xie W, Peng CK, Huang CC, Lin CP, Tsai SJ, Yang AC (2018) Functional brain lateralization in schizophrenia based on the variability of resting-state fMRI signal. Prog Neuro-Psychopharmacol Biol Psychiatry 86:114–121.  https://doi.org/10.1016/j.pnpbp.2018.05.020 Google Scholar
  47. 47.
    Alderson-Day B, Diederen K, Fernyhough C, Ford JM, Horga G, Margulies DS, McCarthy-Jones S, Northoff G, Shine JM, Turner J (2016) Auditory hallucinations and the brain’s resting-state networks: findings and methodological observations. Schizophrenia Bulletin 42(5):1110–1123Google Scholar
  48. 48.
    Alderson-Day B, McCarthy-Jones S, Fernyhough C (2015) Hearing voices in the resting brain: a review of intrinsic functional connectivity research on auditory verbal hallucinations. Neurosci Biobehav Rev 55:78–87Google Scholar
  49. 49.
    Xu Y, Zhuo C, Qin W, Zhu J, Yu C (2015, 2015) Altered spontaneous brain activity in schizophrenia: a meta-analysis and a large-sample study. Biomed Res Int 15(3):1–11Google Scholar
  50. 50.
    Hoptman MJ, Zuo XN, Butler PD, Javitt DC, D’Angelo D, Mauro CJ, Milham MP (2010) Amplitude of low-frequency oscillations in schizophrenia: a resting state fMRI study. Schizophr Res 117(1):13–20Google Scholar
  51. 51.
    Plaze M, Bartrés-Faz D, Martinot JL, Januel D, Bellivier F, Beaurepaire RD, Chanraud S, Andoh J, Lefaucheur JP, Artiges E (2006) Left superior temporal gyrus activation during sentence perception negatively correlates with auditory hallucination severity in schizophrenia patients. Schizophr Res 87(1):109–115Google Scholar
  52. 52.
    Jardri R, Pouchet A, Pins D, Thomas P (2011) Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. Am J Psychiatr 168(1):73–81Google Scholar
  53. 53.
    Homan P, Kindler J, Hauf M, Walther S, Hubl D, Dierks T (2013) Repeated measurements of cerebral blood flow in the left superior temporal gyrus reveal tonic hyperactivity in patients with auditory verbal hallucinations: a possible trait marker. Front Hum Neurosci 7:304Google Scholar
  54. 54.
    Kühn S, Gallinat J (2010) Quantitative meta-analysis on state and trait aspects of auditory verbal hallucinations in schizophrenia. Schizophr Bull 38(4):779–786Google Scholar
  55. 55.
    Holcomb HH, Cascella NG, Thaker GK, Medoff DR (1996) Functional sites of neuroleptic drug action in the human brain: PET/FDG studies with and without haloperidol. Am J Psychiatry 153(1):41Google Scholar
  56. 56.
    Lahti AC, Weiler MA, Holcomb HH, Tamminga CA, Cropsey KL (2009) Modulation of limbic circuitry predicts treatment response to antipsychotic medication: a functional imaging study in schizophrenia. Neuropsychopharmacology 34(13):2675Google Scholar
  57. 57.
    Molina V, Gispert JD, Reig S, Sanz J, Pascau J, Santos A, Desco M, Palomo T (2005) Cerebral metabolic changes induced by clozapine in schizophrenia and related to clinical improvement. Psychopharmacology 178(1):17–26Google Scholar
  58. 58.
    Nenadic I, Dietzek M, Langbein K, Rzanny R, Gussew A, Reichenbach JR, Sauer H, Smesny S (2014) Superior temporal metabolic changes related to auditory hallucinations: a 31P-MR spectroscopy study in antipsychotic-free schizophrenia patients. Brain Struct Funct 219(5):1869–1872Google Scholar
  59. 59.
    Sakai K, Sakamoto R, Okada T, Sugimoto N, Togashi K (2012) DWI based thermometry: the effects of b-values, resolutions, signal-to-noise ratio, and magnet strength. In: Engineering in Medicine and Biology Society (EMBC), 2012 Annual International Conference of the IEEE. IEEE, pp 2291–2293Google Scholar
  60. 60.
    Sparacia G, Sakai K, Yamada K, Giordano G, Coppola R, Midiri M, Grimaldi LM (2017) Assessment of brain core temperature using MR DWI-thermometry in Alzheimer disease patients compared to healthy subjects. Jpn J Radiol 35(4):168–171Google Scholar
  61. 61.
    Sumida K, Sato N, Ota M, Sakai K, Nippashi Y, Sone D, Yokoyama K, Ito K, Maikusa N, Imabayashi E (2015) Intraventricular cerebrospinal fluid temperature analysis using MR diffusion-weighted imaging thermometry in Parkinson’s disease patients, multiple system atrophy patients, and healthy subjects. Brain Behav 5(6):1–5Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Shanghai Key Laboratory of Magnetic Resonance, Key Laboratory of Brain Functional Genomics (MOE & STCSM), Institute of Cognitive NeuroscienceEast China Normal UniversityShanghaiChina
  2. 2.Department of Psychiatry & New York State Psychiatric InstituteColumbia UniversityNew YorkUSA
  3. 3.College of MedicineZhejiang UniversityHangzhouChina
  4. 4.Key Laboratory of Brain Functional Genomics (MOE & STCSM), Institute of Cognitive NeuroscienceEast China Normal UniversityShanghaiChina
  5. 5.Department of Psychiatry, The First Affiliated Hospital, The Key Laboratory of Mental Disorder’s Management of Zhejiang ProvinceZhejiang University School of MedicineHangzhouChina

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