Skip to main content
Top
Gepubliceerd in:

23-05-2018 | Original Paper

Cerebro-Cerebellar Functional Connectivity is Associated with Cerebellar Excitation–Inhibition Balance in Autism Spectrum Disorder

Auteurs: John P. Hegarty II, Dylan J. Weber, Carmen M. Cirstea, David Q. Beversdorf

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 10/2018

Log in om toegang te krijgen
share
DELEN

Deel dit onderdeel of sectie (kopieer de link)

  • Optie A:
    Klik op de rechtermuisknop op de link en selecteer de optie “linkadres kopiëren”
  • Optie B:
    Deel de link per e-mail

Abstract

Atypical functional connectivity (FC) and an imbalance of excitation-to-inhibition (E/I) have been previously reported in cerebro-cerebellar circuits in autism spectrum disorder (ASD). The current investigation used resting state fMRI and proton magnetic resonance spectroscopy (1H-MRS) to examine the relationships between E/I (glutamate + glutamine/GABA) and FC of the dorsolateral prefrontal cortex and posterolateral cerebellar hemisphere from 14 adolescents/adults with ASD and 12 age/sex/IQ-matched controls. In this pilot sample, cerebro-cerebellar FC was positively associated with cerebellar E/I and listening comprehension abilities in individuals with ASD but not controls. Additionally, a subgroup of individuals with ASD and low FC (n = 5) exhibited reduced E/I and impaired listening comprehension. Thus, altered functional coherence of cerebro-cerebellar circuits in ASD may be related with a cerebellar E/I imbalance.
Bijlagen
Alleen toegankelijk voor geautoriseerde gebruikers
Literatuur
go back to reference Aman, M. G., Singh, N. N., Stewart, A. W., & Field, C. J. (1985). The aberrant behavior checklist: A behavior rating scale for the assessment of treatment effects. American Journal of Mental Deficiency, 89(5), 485–491.PubMed Aman, M. G., Singh, N. N., Stewart, A. W., & Field, C. J. (1985). The aberrant behavior checklist: A behavior rating scale for the assessment of treatment effects. American Journal of Mental Deficiency, 89(5), 485–491.PubMed
go back to reference APA. (2013). Diagnostic and statistical manual of mental disorders: DSM-V. Arlington, VA: APA. APA. (2013). Diagnostic and statistical manual of mental disorders: DSM-V. Arlington, VA: APA.
go back to reference Arin, D. M., Bauman, M. L., & Kemper, T. L. (1991). The distribution of Purkinje cell loss in the cerebellum in autism. Neurology, 41(Suppl), 307. Arin, D. M., Bauman, M. L., & Kemper, T. L. (1991). The distribution of Purkinje cell loss in the cerebellum in autism. Neurology, 41(Suppl), 307.
go back to reference Bailey, A., Luthert, P., Dean, A., Harding, B., Janota, I., Montgomery, M., … Lantos, P. (1998). A clinicopathological study of autism. Brain, 121, 889–905.CrossRef Bailey, A., Luthert, P., Dean, A., Harding, B., Janota, I., Montgomery, M., … Lantos, P. (1998). A clinicopathological study of autism. Brain, 121, 889–905.CrossRef
go back to reference Baron-Cohen, S., Ring, H., Wheelwright, S., Bullmore, E., Brammer, M., Simmons, A., & Williams, S. (1999). Social intelligence in the normal and autistic brain: An fMRI study. European Journal of Neuroscience, 11(6), 1891–1898.CrossRef Baron-Cohen, S., Ring, H., Wheelwright, S., Bullmore, E., Brammer, M., Simmons, A., & Williams, S. (1999). Social intelligence in the normal and autistic brain: An fMRI study. European Journal of Neuroscience, 11(6), 1891–1898.CrossRef
go back to reference Bauman, M. L., & Kemper, T. L. (1985). Histoanatomic observations of the brain in early infantile autism. Neurology, 35, 866–874.CrossRef Bauman, M. L., & Kemper, T. L. (1985). Histoanatomic observations of the brain in early infantile autism. Neurology, 35, 866–874.CrossRef
go back to reference Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57(1), 289–300. Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57(1), 289–300.
go back to reference Bottomley, P. A. (1987). Spatial localization in NMR spectroscopy in vivo. Annals of the New York Academy of Sciences, 508(1), 333–348.CrossRef Bottomley, P. A. (1987). Spatial localization in NMR spectroscopy in vivo. Annals of the New York Academy of Sciences, 508(1), 333–348.CrossRef
go back to reference Constantino, J. N., & Gruber, C. P. (2007). Social responsiveness scale (SRS). CA: Western Psychological Services Los Angeles. Constantino, J. N., & Gruber, C. P. (2007). Social responsiveness scale (SRS). CA: Western Psychological Services Los Angeles.
go back to reference Fatemi, S. H., Halt, A. R., Stary, J. M., Kanodia, R., Schulz, S. C., & Realmuto, G. R. (2002). Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices. Biol Psychiatry, 52(8), 805–810.CrossRef Fatemi, S. H., Halt, A. R., Stary, J. M., Kanodia, R., Schulz, S. C., & Realmuto, G. R. (2002). Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices. Biol Psychiatry, 52(8), 805–810.CrossRef
go back to reference Fatemi, S. H., Stary, J. M., Halt, A. R., & Realmuto, G. R. (2001). Dysregulation of Reelin and Bcl-2 proteins in autistic cerebellum. Journal of Autism and Developmental Disorders, 31(6), 529–535.CrossRef Fatemi, S. H., Stary, J. M., Halt, A. R., & Realmuto, G. R. (2001). Dysregulation of Reelin and Bcl-2 proteins in autistic cerebellum. Journal of Autism and Developmental Disorders, 31(6), 529–535.CrossRef
go back to reference Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews, 8, 700–711.CrossRef Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews, 8, 700–711.CrossRef
go back to reference Friedman, S. D., Shaw, D. W., Artru, A. A., Richards, T. L., Gardner, J., Dawson, G., … Dager, S. R. (2003). Regional brain chemical alterations in young children with autism spectrum disorder. Neurology, 60, 100–107.CrossRef Friedman, S. D., Shaw, D. W., Artru, A. A., Richards, T. L., Gardner, J., Dawson, G., … Dager, S. R. (2003). Regional brain chemical alterations in young children with autism spectrum disorder. Neurology, 60, 100–107.CrossRef
go back to reference Gasparovic, C., Song, T., Devier, D., Bockholt, H. J., Caprihan, A., Mullins, P. G., … Morrison, L. A. (2006). Use of tissue water as a concentration reference for proton spectroscopic imaging. Magnetic Resonance in Medicine, 55(6), 1219–1226.CrossRef Gasparovic, C., Song, T., Devier, D., Bockholt, H. J., Caprihan, A., Mullins, P. G., … Morrison, L. A. (2006). Use of tissue water as a concentration reference for proton spectroscopic imaging. Magnetic Resonance in Medicine, 55(6), 1219–1226.CrossRef
go back to reference Guell, X., Hoche, F., & Schmahmann, J. D. (2015). Metalinguistic deficits in patients with cerebellar dysfunction: Empirical support for the dysmetria of though theory. Cerebellum, 14, 50–58.CrossRef Guell, X., Hoche, F., & Schmahmann, J. D. (2015). Metalinguistic deficits in patients with cerebellar dysfunction: Empirical support for the dysmetria of though theory. Cerebellum, 14, 50–58.CrossRef
go back to reference Guerrini, L., Belli, G., Mazzoni, L., Foresti, S., Ginestroni, A., Della Nave, R., … Mascalchi, M. (2009). Impact of cerebrospinal fluid contamination on brain metabolites evaluation with 1H-MR spectroscopy: A single voxel study of the cerebellar vermis in patients with degenerative ataxias. Journal of Magnetic Resonance Imaging, 30(1), 11–17. https://doi.org/10.1002/jmri.21804.CrossRefPubMed Guerrini, L., Belli, G., Mazzoni, L., Foresti, S., Ginestroni, A., Della Nave, R., … Mascalchi, M. (2009). Impact of cerebrospinal fluid contamination on brain metabolites evaluation with 1H-MR spectroscopy: A single voxel study of the cerebellar vermis in patients with degenerative ataxias. Journal of Magnetic Resonance Imaging, 30(1), 11–17. https://​doi.​org/​10.​1002/​jmri.​21804.CrossRefPubMed
go back to reference Hartigan, J. A., & Hartigan, P. M. (1985). The dip test of unimodality. The Annals of Statistics, 13, 70–84.CrossRef Hartigan, J. A., & Hartigan, P. M. (1985). The dip test of unimodality. The Annals of Statistics, 13, 70–84.CrossRef
go back to reference IBM. (2013). IBM SPSS statistics for Macintosh (version 22). Armonk, NY: IBM Corp. IBM. (2013). IBM SPSS statistics for Macintosh (version 22). Armonk, NY: IBM Corp.
go back to reference Ito, H., Mori, K., Harada, M., Hisaoka, S., Toda, Y., Mori, T., … Kagami, S. (2017). A proton magnetic resonance spectroscopic study in autism spectrum disorder using a 3-Tesla clinical magnetic resonance imaging (MRI) system: The anterior cingulate cortex and the left cerebellum. Journal of Child Neurology. https://doi.org/10.1177/0883073817702981.CrossRefPubMed Ito, H., Mori, K., Harada, M., Hisaoka, S., Toda, Y., Mori, T., … Kagami, S. (2017). A proton magnetic resonance spectroscopic study in autism spectrum disorder using a 3-Tesla clinical magnetic resonance imaging (MRI) system: The anterior cingulate cortex and the left cerebellum. Journal of Child Neurology. https://​doi.​org/​10.​1177/​0883073817702981​.CrossRefPubMed
go back to reference Jansen, J. F. A., Backes, W. H., Nicolay, K., & Kooi, M. E. (2006). H MR spectroscopy of the brain: Absolute quantification of metabolites. Radiology, 240(2), 15.CrossRef Jansen, J. F. A., Backes, W. H., Nicolay, K., & Kooi, M. E. (2006). H MR spectroscopy of the brain: Absolute quantification of metabolites. Radiology, 240(2), 15.CrossRef
go back to reference Jenkinson, M., Beckman, C. F., Behrens, T. E., Woolrich, M. W., & Smith, S. M. (2012). FSL. NeuroImage, 62, 782–790.CrossRef Jenkinson, M., Beckman, C. F., Behrens, T. E., Woolrich, M. W., & Smith, S. M. (2012). FSL. NeuroImage, 62, 782–790.CrossRef
go back to reference Jensen, J. E., deB. Frederick, B., & Renshaw, P. F. (2005). Grey and white matter GABA level differences in the human brain using two-dimensional, J-resolved spectroscopic imaging. NMR in Biomedicine, 18(8), 570–576.CrossRef Jensen, J. E., deB. Frederick, B., & Renshaw, P. F. (2005). Grey and white matter GABA level differences in the human brain using two-dimensional, J-resolved spectroscopic imaging. NMR in Biomedicine, 18(8), 570–576.CrossRef
go back to reference Kingma, A., Mooij, J. J. A., Metzemaekers, J. D. M., & Leeuw, J. A. (1994). Transient mutism and speech disorders after posterior fossa surgery in children with brain tumours. Acta Neurochirurgica, 131(1–2), 74–79.CrossRef Kingma, A., Mooij, J. J. A., Metzemaekers, J. D. M., & Leeuw, J. A. (1994). Transient mutism and speech disorders after posterior fossa surgery in children with brain tumours. Acta Neurochirurgica, 131(1–2), 74–79.CrossRef
go back to reference Kreis, R. (2004). Issues of spectral quality in clinical 1 H-magnetic resonance spectroscopy and a gallery of artefacts. NMR in Biomedicine, 17, 361–381.CrossRef Kreis, R. (2004). Issues of spectral quality in clinical 1 H-magnetic resonance spectroscopy and a gallery of artefacts. NMR in Biomedicine, 17, 361–381.CrossRef
go back to reference Le Couteur, A., Lord, C., & Rutter, M. (2003). The autism diagnostic interview-revised (ADI-R). Los Angeles, CA: Western Psychological Services. Le Couteur, A., Lord, C., & Rutter, M. (2003). The autism diagnostic interview-revised (ADI-R). Los Angeles, CA: Western Psychological Services.
go back to reference Lord, C., Risi, S., Lambrecht, L., Cook, E. H. Jr., Leventhal, B. L., DiLavore, P. C., … Rutter, M. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.CrossRef Lord, C., Risi, S., Lambrecht, L., Cook, E. H. Jr., Leventhal, B. L., DiLavore, P. C., … Rutter, M. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.CrossRef
go back to reference 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.CrossRef 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.CrossRef
go back to reference Mazziotta, J., Toga, A., Evans, A. C., Fox, P., Lancaster, J., Zilles, K., … Mazoyer, B. (2001). A probabilistic atlas and reference system for the human brain: International consortium for brain mapping (ICBM). Philosophical Transactions of the Royal Society B, 356, 1293–1322.CrossRef Mazziotta, J., Toga, A., Evans, A. C., Fox, P., Lancaster, J., Zilles, K., … Mazoyer, B. (2001). A probabilistic atlas and reference system for the human brain: International consortium for brain mapping (ICBM). Philosophical Transactions of the Royal Society B, 356, 1293–1322.CrossRef
go back to reference Mescher, M., Merkle, H., Kirsch, J., Garwood, M., & Gruetter, R. (1998). Simultaneous in vivo spectral editing and water suppression. NMR in Biomedicine, 11, 266–272.CrossRef Mescher, M., Merkle, H., Kirsch, J., Garwood, M., & Gruetter, R. (1998). Simultaneous in vivo spectral editing and water suppression. NMR in Biomedicine, 11, 266–272.CrossRef
go back to reference Mostofsky, S. H., Powell, S. K., Simmonds, D. J., Goldberg, M. C., Caffo, B., & Pekar, J. J. (2009). Decreased connectivity and cerebellar activity in autism during motor task performance. Brain, 132, 2413–2425.CrossRef Mostofsky, S. H., Powell, S. K., Simmonds, D. J., Goldberg, M. C., Caffo, B., & Pekar, J. J. (2009). Decreased connectivity and cerebellar activity in autism during motor task performance. Brain, 132, 2413–2425.CrossRef
go back to reference Near, J., Simpson, R., Cowen, P., & Jezzard, P. (2011). Efficient γ-aminobutyric acid editing at 3T without macromolecule contamination: MEGA-SPECIAL. NMR in Biomedicine, 24(10), 1277–1285.CrossRef Near, J., Simpson, R., Cowen, P., & Jezzard, P. (2011). Efficient γ-aminobutyric acid editing at 3T without macromolecule contamination: MEGA-SPECIAL. NMR in Biomedicine, 24(10), 1277–1285.CrossRef
go back to reference Nicoletti, F., Wroblewski, J. T., Novelli, A., Alho, H., Guidotti, A., & Costa, E. (1986). The activation of inositol phospholipid metabolism as a signal- transducing system for excitatory amino acids in primary cultures of cerebellar granule cells. The Journal of Neuroscience, 6(7), 1905.CrossRef Nicoletti, F., Wroblewski, J. T., Novelli, A., Alho, H., Guidotti, A., & Costa, E. (1986). The activation of inositol phospholipid metabolism as a signal- transducing system for excitatory amino acids in primary cultures of cerebellar granule cells. The Journal of Neuroscience, 6(7), 1905.CrossRef
go back to reference Provencher, S. W. (2001). Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR in Biomedicine, 14(4), 260–264.CrossRef Provencher, S. W. (2001). Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR in Biomedicine, 14(4), 260–264.CrossRef
go back to reference Purcell, A. E., Jeon, O. H., Zimmerman, A. W., Blue, M. E., & Pevsner, J. (2001). Postmortem brain abnormalities of the glutamate neurotransmitter system in autism. Neurology, 57, 1618–1628.CrossRef Purcell, A. E., Jeon, O. H., Zimmerman, A. W., Blue, M. E., & Pevsner, J. (2001). Postmortem brain abnormalities of the glutamate neurotransmitter system in autism. Neurology, 57, 1618–1628.CrossRef
go back to reference Ritvo, E. R., Freeman, B. J., Scheibel, A. B., Duong, T., Robinson, H., Guthrie, D., & Ritvo, A. (1986). Lower Purkinje cell counts in the cerebella of four autitic subjects: Initial findings of the UCLA-NSAC autopsy research report. American Journal of Psychiatry, 143, 862–866.CrossRef Ritvo, E. R., Freeman, B. J., Scheibel, A. B., Duong, T., Robinson, H., Guthrie, D., & Ritvo, A. (1986). Lower Purkinje cell counts in the cerebella of four autitic subjects: Initial findings of the UCLA-NSAC autopsy research report. American Journal of Psychiatry, 143, 862–866.CrossRef
go back to reference Rothman, D. L., Petroff, O. A., Behar, K. L., & Mattson, R. H. (1993). Localized 1H NMR measurements of gamma-aminobutyric acid in human brain in vivo. Proceedings of the National Academy of Sciences of the United States of America 90(12), 5662–5666.CrossRef Rothman, D. L., Petroff, O. A., Behar, K. L., & Mattson, R. H. (1993). Localized 1H NMR measurements of gamma-aminobutyric acid in human brain in vivo. Proceedings of the National Academy of Sciences of the United States of America 90(12), 5662–5666.CrossRef
go back to reference Schmahmann, J. D., & Sherman, J. C. (1998). The cerebellar cognitive affective syndrome. Brain, 121, 561–579.CrossRef Schmahmann, J. D., & Sherman, J. C. (1998). The cerebellar cognitive affective syndrome. Brain, 121, 561–579.CrossRef
go back to reference Segovia, G., Del Arco, A., Prieto, L., & Mora, F. (2001). Glutamate-glutamine cycle and aging in striatum of the awake rat: Effects of a glutamate transporter blocker. Neurochemical Research, 26(1), 37–41.CrossRef Segovia, G., Del Arco, A., Prieto, L., & Mora, F. (2001). Glutamate-glutamine cycle and aging in striatum of the awake rat: Effects of a glutamate transporter blocker. Neurochemical Research, 26(1), 37–41.CrossRef
go back to reference Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckman, C. F., Behrens, T. E., Johansen-Berg, H., … Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Supplement 1), S208–S219.CrossRef Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckman, C. F., Behrens, T. E., Johansen-Berg, H., … Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Supplement 1), S208–S219.CrossRef
go back to reference Song, X.-W., Dong, Z.-Y., Long, X.-Y., Li, S.-F., Zuo, X.-N., Zhu, C.-Z., … Zang, Y.-F. (2011). REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE, 6(9), E25031.CrossRef Song, X.-W., Dong, Z.-Y., Long, X.-Y., Li, S.-F., Zuo, X.-N., Zhu, C.-Z., … Zang, Y.-F. (2011). REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE, 6(9), E25031.CrossRef
go back to reference Stoodley, C. J., Valera, E. M., & Schmahmann, J. D. (2012). Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study. NeuroImage, 59(2), 1560–1570.CrossRef Stoodley, C. J., Valera, E. M., & Schmahmann, J. D. (2012). Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study. NeuroImage, 59(2), 1560–1570.CrossRef
go back to reference Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme.
go back to reference Tedesco, A. M., Chiricozzi, F. R., Clausi, S., Lupo, M., Molinari, M., & Leggio, M. G. (2011). The cerebellar cognitive profile. Brain, 134(12), 3672–3686.CrossRef Tedesco, A. M., Chiricozzi, F. R., Clausi, S., Lupo, M., Molinari, M., & Leggio, M. G. (2011). The cerebellar cognitive profile. Brain, 134(12), 3672–3686.CrossRef
go back to reference Tsai, S.-Y., Fang, C.-H., Wu, T.-Y., & Lin, Y.-R. (2016). Effects of frequency drift on the quantification of gamma-aminobutyric acid using MEGA-PRESS. Scientific Reports, 6, 24564.CrossRef Tsai, S.-Y., Fang, C.-H., Wu, T.-Y., & Lin, Y.-R. (2016). Effects of frequency drift on the quantification of gamma-aminobutyric acid using MEGA-PRESS. Scientific Reports, 6, 24564.CrossRef
go back to reference Wechsler, D. (1999). WASI manual. San Antonio: Psychological Corporation. Wechsler, D. (1999). WASI manual. San Antonio: Psychological Corporation.
go back to reference Wiig, E. H., & Secord, W. (1989). Test of language competence (TLC): Expanded edition. San Antonio: Psychological Corporation. Wiig, E. H., & Secord, W. (1989). Test of language competence (TLC): Expanded edition. San Antonio: Psychological Corporation.
go back to reference Zhang, Y., Brady, M., & Smith, S. (2001). Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Transactions on Medical Imaging, 20(1), 45–57.CrossRef Zhang, Y., Brady, M., & Smith, S. (2001). Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Transactions on Medical Imaging, 20(1), 45–57.CrossRef
Metagegevens
Titel
Cerebro-Cerebellar Functional Connectivity is Associated with Cerebellar Excitation–Inhibition Balance in Autism Spectrum Disorder
Auteurs
John P. Hegarty II
Dylan J. Weber
Carmen M. Cirstea
David Q. Beversdorf
Publicatiedatum
23-05-2018
Uitgeverij
Springer US
Gepubliceerd in
Journal of Autism and Developmental Disorders / Uitgave 10/2018
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI
https://doi.org/10.1007/s10803-018-3613-y