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Contributions of magnetic resonance spectroscopy to understanding development: Potential applications in the study of adolescent alcohol use and abuse

Published online by Cambridge University Press:  12 March 2014

Julia E. Cohen-Gilbert ,
J. Eric Jensen  and
Marisa M. Silveri
Julia E. Cohen-Gilbert*
Affiliation:
Neurodevelopmental Laboratory on Addictions and Mental Health McLean Hospital Harvard Medical School
J. Eric Jensen
Affiliation:
McLean Hospital Harvard Medical School
Marisa M. Silveri
Affiliation:
Neurodevelopmental Laboratory on Addictions and Mental Health McLean Hospital Harvard Medical School
*
Address correspondence and reprint requests to: Julia E. Cohen-Gilbert, McLean Imaging Center, McLean Hospital, 115 Mill Street, Belmont, MA 02478; E-mail: [email protected].
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Abstract

A growing body of research has documented structural and functional brain development during adolescence, yet little is known about neurochemical changes that occur during this important developmental period. Magnetic resonance spectroscopy (MRS) is a well-developed technology that permits the in vivo quantification of multiple brain neurochemicals relevant to neuronal health and functioning. However, MRS technology has been underused in exploring normative developmental changes during adolescence and the onset of alcohol and drug use and abuse during this developmental period. This review begins with a brief overview of normative cognitive and neurobiological development during adolescence, followed by an introduction to MRS principles. The subsequent sections provide a comprehensive review of the existing MRS studies of development and cognitive functioning in healthy children and adolescents. The final sections of this article address the potential application of MRS in identifying neurochemical predictors and consequences of alcohol use and abuse in adolescence. MRS studies of adolescent populations hold promise for advancing our understanding of neurobiological risk factors for psychopathology by identifying the biochemical signatures associated with healthy brain development, as well as neurobiological and cognitive correlates of alcohol and substance use and abuse.

Type
Regular Articles
Information
Development and Psychopathology , Volume 26 , Issue 2 , May 2014 , pp. 405 - 423
Copyright
Copyright © Cambridge University Press 2014 

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References

Abe, C., Mon, A., Durazzo, T. C., Pennington, D. L., Schmidt, T. P., & Meyerhoff, D. J. (2012). Polysubstance and alcohol dependence: Unique abnormalities of magnetic resonance-derived brain metabolite levels. Drug and Alcohol Dependence, 130, 30–37.Google Scholar
Auer, D. P., Gossl, C., Schirmer, T., & Czisch, M. (2001). Improved analysis of 1H-MR spectra in the presence of mobile lipids. Magnetic Resonance in Medicine, 46, 615–618.CrossRefGoogle ScholarPubMed
Barker, P. B., Breiter, S. N., Soher, B. J., Chatham, J. C., Forder, J. R., Samphilipo, M. A., et al. (1994). Quantitative proton spectroscopy of canine brain: In vivo and in vitro correlations. Magnetic Resonance in Medicine, 32, 157–163.CrossRefGoogle ScholarPubMed
Barnea-Goraly, N., Menon, V., Eckert, M., Tamm, L., Bammer, R., Karchemskiy, A., et al. (2005). White matter development during childhood and adolescence: A cross-sectional diffusion tensor imaging study. Cerebral Cortex, 15, 1848–1854.Google Scholar
Bava, S., Thayer, R., Jacobus, J., Ward, M., Jernigan, T. L., & Tapert, S. F. (2010). Longitudinal characterization of white matter maturation during adolescence. Brain Research, 1327, 38–46.CrossRefGoogle ScholarPubMed
Behar, K. L., & Rothman, D. L. (2001). In vivo nuclear magnetic resonance studies of glutamate-gamma-aminobutyric acid-glutamine cycling in rodent and human cortex: The central role of glutamine. Journal of Nutrition, 131(Suppl. 9), 2498S–2504S; discussion 2523S–2524S.Google Scholar
Behar, K. L., Rothman, D. L., Petersen, K. F., Hooten, M., Delaney, R., Petroff, O. A., et al. (1999). Preliminary evidence of low cortical GABA levels in localized 1H-MR spectra of alcohol-dependent and hepatic encephalopathy patients. American Journal of Psychiatry, 156, 952–954.Google Scholar
Behar, K. L., Rothman, D. L., Spencer, D. D., & Petroff, O. A. (1994). Analysis of macromolecule resonances in 1H NMR spectra of human brain. Magnetic Resonance in Medicine, 32, 294–302.Google Scholar
Berridge, M. J., & Irvine, R. F. (1989). Inositol phosphates and cell signalling. Nature, 341, 197–205.CrossRefGoogle ScholarPubMed
Bessman, S. P., & Geiger, P. J. (1981). Transport of energy in muscle: The phosphorylcreatine shuttle. Science, 211, 448–452.Google Scholar
Birken, D. L., & Oldendorf, W. H. (1989). N-Acetyl-L-aspartic acid: A literature review of a compound prominent in 1H-NMR spectroscopic studies of brain. Neuroscience and Biobehavioral Reviews, 13, 23–31.Google Scholar
Blakemore, S.-J., & Choudhury, S. (2006). Development of the adolescent brain: Implications for executive function and social cognition. Journal of Child Psychology and Psychiatry, 47, 296–312.Google Scholar
Boesch, C., Gruetter, R., Martin, E., Duc, G., & Wuthrich, K. (1989). Variations in the in vivo P-31 MR spectra of the developing human brain during postnatal life: Work in progress. Radiology, 172, 197–199.Google Scholar
Bovey, F. A., Jelinski, L., & Mirau, P. A. (1988). Nuclear magnetic resonance spectroscopy. San Diego, CA: Academic Press.Google Scholar
Boy, F., Evans, C. J., Edden, R. A. E., Lawrence, A. D., Singh, K. D., Husain, M., et al. (2011). Dorsolateral prefrontal gamma-aminobutyric acid in men predicts individual differences in rash impulsivity. Biological Psychiatry, 70, 866–872.Google Scholar
Boy, F., Evans, C. J., Edden, R. A., Singh, K. D., Husain, M., & Sumner, P. (2010). Individual differences in subconscious motor control predicted by GABA concentration in SMA. Current Biology, 20, 1779–1785.Google Scholar
Brand, A., Richter-Landsberg, C., & Leibfritz, D. (1993). Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Developmental Neuroscience, 15, 289–298.Google Scholar
Brown, T. R., Kincaid, B. M., & Ugurbil, K. (1982). NMR chemical shift imaging in three dimensions. Proceedings of the National Academy of Sciences, 79, 3523–3526.Google Scholar
Buckley, P. F., Moore, C., Long, H., Larkin, C., Thompson, P., Mulvany, F., et al. (1994). 1H-magnetic resonance spectroscopy of the left temporal and frontal lobes in schizophrenia: Clinical, neurodevelopmental, and cognitive correlates. Biological Psychiatry, 36, 792–800.Google Scholar
Casey, B. J., Jones, R. M., & Hare, T. A. (2008). The adolescent brain. Annals of the New York Academy of Sciences, 1124, 111–126.Google Scholar
Casey, B. J., Trainor, R. J., Orendi, J. L., Schubert, A. B., Nystrom, L. E., Giedd, J. N., et al. (1997). A developmental functional MRI study of prefrontal activation during performance of a go-no-go task. Journal of Cognitive Neuroscience, 9, 835–847.Google Scholar
Catani, M., Cherubini, A., Howard, R., Tarducci, R., Pelliccioli, G. P., Piccirilli, M., et al. (2001). (1)H-MR spectroscopy differentiates mild cognitive impairment from normal brain aging. NeuroReport, 12, 2315–2317.Google Scholar
Charlton, R. A., McIntyre, D. J. O., Howe, F. A., Morris, R. G., & Markus, H. S. (2007). The relationship between white matter brain metabolites and cognition in normal aging: The GENIE study. Brain Research, 1164, 108–116.Google Scholar
Chen, X., Pavan, M., Heinzer-Schweizer, S., Boesiger, P., & Henning, A. (2012). Optically transmitted and inductively coupled electric reference to access in vivo concentrations for quantitative proton-decoupled 13C magnetic resonance spectroscopy. Magnetic Resonance in Medicine, 67, 1–7.CrossRefGoogle ScholarPubMed
Choi, C. G., Ko, T. S., Lee, H. K., Lee, J. H., & Suh, D. C. (2000). Localized proton MR spectroscopy of the allocortex and isocortex in healthy children. American Journal of Neuroradiology, 21, 1354–1358.Google Scholar
Chugani, H. T. (1998). A critical period of brain development: Studies of cerebral glucose utilization with PET. Preventive Medicine, 27, 184–188.Google Scholar
Cohen-Gilbert, J. E., & Thomas, K. M. (2013). Inhibitory control during emotional distraction across adolescence and early adulthood. Child Development, 84, 1954–1966.Google Scholar
Costa, M. O., Lacerda, M. T., Garcia Otaduy, M. C., Cerri, G. G., & Da Costa Leite, C. (2002). Proton magnetic resonance spectroscopy: Normal findings in the cerebellar hemisphere in childhood. Pediatric Radiology, 32, 787–792.Google Scholar
Crone, E. A., Wendelken, C., Donahue, S., van Leijenhorst, L., & Bunge, S. (2006). Neurocognitive development of the ability to manipulate information in working memory. Proceedings of the National Academy of Sciences, 103, 9315–9320.CrossRefGoogle ScholarPubMed
Dahl, R. E. (2001). Affect regulation, brain development and behavioral/emotional health in adolescence. CNS Spectrums, 6, 60–72.CrossRefGoogle ScholarPubMed
Davanzo, P., Yue, K., Thomas, M. A., Belin, T., Mintz, J., Venkatraman, T. N., et al. (2003). Proton magnetic resonance spectroscopy of bipolar disorder versus intermittent explosive disorder in children and adolescents. American Journal of Psychiatry, 160, 1442–1452.Google Scholar
DeBellis, M. D., Clark, D. B., Beers, S. R., Soloff, P. H., Boring, A. M., Hall, J., et al. (2000). Hippocampal volume in adolescent-onset alcohol use disorders. American Journal of Psychiatry, 157, 737–744.Google Scholar
de Graaf, R. A. (2002). In vivo NMR spectroscopy: Principles and techniques (2nd ed.). Chichester: Wiley.Google Scholar
Demougeot, C., Marie, C., Giroud, M., & Beley, A. (2004). N-Acetylaspartate: A literature review of animal research on brain ischaemia. Journal of Neurochemistry, 90, 776–783.Google Scholar
Downes, C. P., & Macphee, C. H. (1990). Myo-inositol metabolites as cellular signals. European Journal of Biochemistry, 193, 1–18.Google Scholar
Durston, S., Davidson, M. C., Tottenham, N., Galvan, A., Spicer, J., Fossella, J. A., et al. (2006). A shift from diffuse to focal cortical activity with development. Developmental Science, 9, 1–20.CrossRefGoogle ScholarPubMed
Eaton, D. K., Kann, L., Kinchen, S., Ross, J., Hawkins, J., Harris, W. A., et al. (2006). Youth risk behavior surveillance—United States, 2005. Journal of School Health, 76, 353–372.Google Scholar
Ernst, M., Nelson, E. E., Jazbec, S., McClure, E. B., Monk, C. S., Leibenluft, E., et al. (2005). Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. NeuroImage, 25, 1279–1291.Google Scholar
Fayed, N., & Modrego, P. J. (2005). Comparative study of cerebral white matter in autism and attention-deficit/hyperactivity disorder by means of magnetic resonance spectroscopy. Academic Radiology, 12, 566–569.Google Scholar
Ferguson, K. J., MacLullich, A. M. J., Marshall, I., Deary, I. J., Starr, J. M., Seckl, J. R., et al. (2002). Magnetic resonance spectroscopy and cognitive function in healthy elderly men. Brain, 125, 2743–2749.Google Scholar
Gabbay, V., Mao, X., Klein, R. G., Ely, B. A., Babb, J. S., Panzer, A. M., et al. (2012). Anterior cingulate cortex gamma-aminobutyric acid in depressed adolescents: Relationship to anhedonia. Archives of General Psychiatry, 69, 139–149.CrossRefGoogle ScholarPubMed
Galvan, A., Hare, T. A., Parra, C. E., Penn, J., Voss, H., Glover, G., et al. (2006). Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. Journal of Neuroscience, 26, 6885–6892.CrossRefGoogle ScholarPubMed
Giedd, J. N., Blumenthal, J., Jeffries, N. O., Castellanos, F. X., Liu, H., Zijdenbos, A., et al. (1999). Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience, 2, 861–863.Google Scholar
Gimenez, M., Junque, C., Narberhaus, A., Caldu, X., Segarra, D., Vendrell, P., et al. (2004). Medial temporal MR spectroscopy is related to memory performance in normal adolescent subjects. NeuroReport, 15, 703–707.Google Scholar
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., et al. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences, 101, 8174–8179.CrossRefGoogle ScholarPubMed
Goldstein, G., Panchalingam, K., McClure, R. J., Stanley, J. A., Calhoun, V. D., Pearlson, G. D., et al. (2009). Molecular neurodevelopment: An in vivo 31P-1H MRSI study. Journal of the International Neuropsychological Society, 15, 671–683.Google Scholar
Gomez, R., Behar, K. L., Watzl, J., Weinzimer, S. A., Gulanski, B., Sanacora, G., et al. (2011). Intravenous ethanol infusion decreases human cortical gamma-aminobutyric acid and N-acetylaspartate as measured with proton magnetic resonance spectroscopy at 4 Tesla. Biological Psychiatry, 71, 239–246.Google Scholar
Grachev, I. D., & Apkarian, A. V. (2000). Chemical heterogeneity of the living human brain: A proton MR spectroscopy study on the effects of sex, age, and brain region. NeuroImage, 11, 554–563.Google Scholar
Grant, B. F., & Dawson, D. A. (1997). Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: Results from the National Longitudinal Alcohol Epidemiologic Survey. Journal of Substance Abuse, 9, 103–110.CrossRefGoogle ScholarPubMed
Gyulai, L., Roth, Z., Leigh, J. S. Jr., & Chance, B. (1985). Bioenergetic studies of mitochondrial oxidative phosphorylation using 31phosphorus NMR. Journal of Biological Chemistry, 260, 3947–3954.Google Scholar
Hanaoka, S., Takashima, S., & Morooka, K. (1998). Study of the maturation of the child's brain using 31P-MRS. Pediatric Neurology, 18, 305–310.Google Scholar
Hare, T. A., Tottenham, N., Galvan, A., Voss, H. U., Glover, G. H., & Casey, B. J. (2008). Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biological Psychiatry, 63, 927–934.Google Scholar
Harris, G. J., Jaffin, S. K., Hodge, S. M., Kennedy, D., Caviness, V. S., Marinkovic, K., et al. (2008). Frontal white matter and cingulum diffusion tensor imaging deficits in alcoholism. Alcoholism: Clinical and Experimental Research, 32, 1001–1013.CrossRefGoogle ScholarPubMed
Heinzer-Schweizer, S., De Zanche, N., Pavan, M., Mens, G., Sturzenegger, U., Henning, A., et al. (2010). In-vivo assessment of tissue metabolite levels using 1H MRS and the Electric REference To access In vivo Concentrations (ERETIC) method. NMR in Biomedicine, 23, 406–413.Google Scholar
Hill, S. Y., Wang, S., Kostelnik, B., Carter, H., Holmes, B., McDermott, M., et al. (2009). Disruption of orbitofrontal cortex laterality in offspring from multiplex alcohol dependence families. Biological Psychiatry, 65, 129–136.Google Scholar
Hooper, C. J., Luciana, M., Conklin, H. M., & Yarger, R. S. (2004). Adolescents' performance on the Iowa Gambling Task: Implications for the development of decision making and ventromedial prefrontal cortex. Developmental Psychology, 40, 1148–1158.CrossRefGoogle ScholarPubMed
Horska, A., Kaufmann, W. E., Brant, L. J., Naidu, S., Harris, J. C., & Barker, P. B. (2002). In vivo quantitative proton MRSI study of brain development from childhood to adolescence. Journal of Magnetic Resonance Imaging, 15, 137–143.Google Scholar
Huizinga, M., Dolan, C. V., & van der Molen, M. W. (2006). Age-related change in executive function: Developmental trends and a latent variable analysis. Neuropsychologia, 44, 2017–2036.Google Scholar
Hüppi, P. S., Posse, S., Lazeyras, F., Burri, R., Bossi, E., & Herschkowitz, N. (1991). Magnetic resonance in preterm and term newborns: 1H spectroscopy in developing human brain. Pediatric Research, 30, 574–578.Google Scholar
Inglese, M., Rusinek, H., George, I. C., Babb, J. S., Grossman, R. I., & Gonen, O. (2008). Global average gray and white matter N-acetylaspartate concentration in the human brain. NeuroImage, 41, 270–276.Google Scholar
Jensen, J. E., Frederick, B. 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, 570–576.Google Scholar
Jensen, J. E., Licata, S. C., Ongur, D., Friedman, S. D., Prescot, A. P., Henry, M. E., et al. (2009). Quantification of J-resolved proton spectra in two-dimensions with LCModel using GAMMA-simulated basis sets at 4 Tesla. NMR in Biomedicine, 22, 762–769.Google Scholar
Johnstone, S. J., Pleffer, C. B., Barry, R. J., Clarke, A. R., & Smith, J. L. (2005). Development of inhibitory processing during the go/nogo task: A behavioral and event-related potential study of children and adults. Journal of Psychophysiology, 19, 11–23.Google Scholar
Jung, R. E., Brooks, W. M., Yeo, R. A., Chiulli, S. J., Weers, D. C., & Sibbitt, W. L. (1999). Biochemical markers of intelligence: A proton MR spectroscopy study of normal human brain. Proceedings: Biological Sciences, 266, 1375–1379.Google Scholar
Jung, R. E., Gasparovic, C., Chavez, R. S., Caprihan, A., Barrow, R., & Yeo, R. A. (2009). Imaging intelligence with proton magnetic resonance spectroscopy. Intelligence, 37, 192–198.Google Scholar
Jung, R. E., Haier, R. J., Yeo, R. A., Rowland, L. M., Petropoulos, H., Levine, A. S., et al. (2005). Sex differences in N-acetylaspartate correlates of general intelligence: An 1H-MRS study of normal human brain. NeuroImage, 26, 965–972.Google Scholar
Jung, R. E., Yeo, R. A., Chiulli, S. J., Sibbitt, W. L. Jr., & Brooks, W. M. (2000). Myths of neuropsychology: Intelligence, neurometabolism, and cognitive ability. Clinical Neuropsychologist, 14, 535.Google Scholar
Kadota, T., Horinouchi, T., & Kuroda, C. (2001). Development and aging of the cerebrum: Assessment with proton MR spectroscopy. American Journal of Neuroradiology, 22, 128–135.Google Scholar
Kantarci, K., Smith, G. E., Ivnik, R. J., Petersen, R. C., Boeve, B. F., Knopman, D. S., et al. (2002). 1H magnetic resonance spectroscopy, cognitive function, and apolipoprotein E genotype in normal aging, mild cognitive impairment and Alzheimer's disease. Journal of the International Neuropsychological Society, 8, 934–942.Google Scholar
Keltner, J. R., Wald, L. L., Frederick, B. D., & Renshaw, P. F. (1997). In vivo detection of GABA in human brain using a localized double-quantum filter technique. Magnetic Resonance in Medicine, 37, 366–371.Google Scholar
Kemp, G. J. (2000). Non-invasive methods for studying brain energy metabolism: What they show and what it means. Developmental Neuroscience, 22, 418–428.Google Scholar
Kim, H., McGrath, B. M., & Silverstone, P. H. (2005). A review of the possible relevance of inositol and the phosphatidylinositol second messenger system (PI-cycle) to psychiatric disorders—Focus on magnetic resonance spectroscopy (MRS) studies. Human Psychopharmacology, 20, 309–326.Google Scholar
Kreis, R., Ernst, T., & Ross, B. D. (1993). Development of the human brain: In vivo quantification of metabolite and water content with proton magnetic resonance spectroscopy. Magnetic Resonance in Medicine, 30, 424–437.Google Scholar
Krupitsky, E. M., Rudenko, A. A., Burakov, A. M., Slavina, T. Y., Grinenko, A. A., Pittman, B., et al. (2007). Antiglutamatergic strategies for ethanol detoxification: Comparison with placebo and diazepam. Alcoholism: Clinical and Experimental Research, 31, 604–611.Google Scholar
Krystal, J. H., Petrakis, I. L., Limoncelli, D., Webb, E., Gueorgueva, R., D'Souza, D. C., et al. (2003). Altered NMDA glutamate receptor antagonist response in recovering ethanol-dependent patients. Neuropsychopharmacology, 28, 2020–2028.CrossRefGoogle ScholarPubMed
Krystal, J. H., Petrakis, I. L., Mason, G., Trevisan, L., & D'Souza, D. C. (2003). N-methyl-D-aspartate glutamate receptors and alcoholism: Reward, dependence, treatment, and vulnerability. Pharmacology & Therapeutics, 99, 79–94.Google Scholar
Krystal, J. H., Staley, J., Mason, G., Petrakis, I. L., Kaufman, J., Harris, R. A., et al. (2006). Gamma-aminobutyric acid type A receptors and alcoholism: Intoxication, dependence, vulnerability, and treatment. Archives of General Psychiatry, 63, 957–968.Google Scholar
Licata, S. C., Jensen, J., Penetar, D., Prescot, A., Lukas, S., & Renshaw, P. (2009). A therapeutic dose of zolpidem reduces thalamic GABA in healthy volunteers: A proton MRS study at 4 T. Psychopharmacology, 203, 819–829.Google Scholar
Liston, C., Watts, R., Tottenham, N., Davidson, M. C., Niogi, S., Ulug, A. M., et al. (2006). Frontostriatal microstructure modulates efficient recruitment of cognitive control. Cerebral Cortex, 16, 553–560.CrossRefGoogle ScholarPubMed
Luna, B., Padmanabhan, A., & O'Hearn, K. (2010). What has fMRI told us about the development of cognitive control through adolescence? Brain and Cognition, 72, 101–113.Google Scholar
Lyoo, I. K., Yoon, S. J., Musen, G., Simonson, D. C., Weinger, K., Bolo, N., et al. (2009). Altered prefrontal glutamate-glutamine-{gamma}-aminobutyric acid levels and relation to low cognitive performance and depressive symptoms in type 1 diabetes mellitus. Archives of General Psychiatry, 66, 878.Google Scholar
Mangia, S., Tkac, I., Gruetter, R., De Moortele, V., Giove, F., Maraviglia, B., et al. (2006). Sensitivity of single-voxel 1H-MRS in investigating the metabolism of the activated human visual cortex at 7 T. Magnetic Resonance Imaging, 24, 343–348.Google Scholar
Mason, G. F., Petrakis, I. L., de Graaf, R. A., Gueorguieva, R., Guidone, E., Coric, V., et al. (2006). Cortical gamma-aminobutyric acid levels and the recovery from ethanol dependence: Preliminary evidence of modification by cigarette smoking. Biological Psychiatry, 59, 85–93.Google Scholar
McCormick, D. A. (1989). GABA as an inhibitory neurotransmitter in human cerebral cortex. Journal of Neurophysiology, 62, 1018–1027.Google Scholar
McQueeny, T., Schweinsburg, B. C., Schweinsburg, A. D., Jacobus, J., Bava, S., Frank, L. R., et al. (2009). Altered white matter integrity in adolescent binge drinkers. Alcoholism: Clinical and Experimental Research, 33, 1278–1285.Google Scholar
Mekle, R., Mlynárik, V., Gambarota, G., Hergt, M., Krueger, G., & Gruetter, R. (2009). MR spectroscopy of the human brain with enhanced signal intensity at ultrashort echo times on a clinical platform at 3T and 7T. Magnetic Resonance in Medicine, 61, 1279–1285.Google Scholar
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.Google Scholar
Meyerhoff, D. J., Durazzo, T. C., & Ende, G. (2011). Chronic alcohol consumption, abstinence and relapse: Brain proton magnetic resonance spectroscopy studies in animals and humans. Behavioral Neurobiology of Alcohol Addiction, 13, 511–540.CrossRefGoogle Scholar
Miller, B. L. (1991). A review of chemical issues in 1H NMR spectroscopy: N -acetyl-l-aspartate, creatine and choline. NMR in Biomedicine, 4, 47–52.Google Scholar
Moffett, J. R., Ross, B., Arun, P., Madhavarao, C. N., & Namboodiri, A. M. (2007). N-Acetylaspartate in the CNS: From neurodiagnostics to neurobiology. Progress in Neurobiology, 81, 89–131.Google Scholar
Mon, A., Durazzo, T. C., & Meyerhoff, D. J. (2012). Glutamate, GABA, and other cortical metabolite concentrations during early abstinence from alcohol and their associations with neurocognitive changes. Drug and Alcohol Dependence, 125, 27–36.CrossRefGoogle ScholarPubMed
Moore, C. M., Breeze, J. L., Kukes, T. J., Rose, S. L., Dager, S. R., Cohen, B. M., et al. (1999). Effects of myo-inositol ingestion on human brain myo-inositol levels: A proton magnetic resonance spectroscopic imaging study. Biological Psychiatry, 45, 1197–1202.CrossRefGoogle Scholar
Moss, H. B., & Talagala, S. L. (1997). 31P magnetic resonance spectroscopy of normal peripubertal children: Effects of sex and fronto-occipital location. Proceedings of the 5th Annual Meeting of the International Society for Magnetic Resonance in Medicine (Vol. 2, p. 1219). Berkeley, CA: International Society for Magnetic Resonance in Medicine.Google Scholar
Moss, H. B., Talagala, S. L., & Kirisci, L. (1997). Phosphorus-31 magnetic resonance brain spectroscopy of children at risk for a substance use disorder: Preliminary results. Psychiatry Research: Neuroimaging, 76, 101–112.Google Scholar
Nigg, J. T., Wong, M. M., Martel, M. M., Jester, J. M., Puttler, L. I., Glass, J. M., et al. (2006). Poor response inhibition as a predictor of problem drinking and illicit drug use in adolescents at risk for alcoholism and other substance use disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 45, 468–475.Google Scholar
Nioka, S., Smith, D. S., Chance, B., Subramanian, H. V., Butler, S., & Katzenberg, M. (1990). Oxidative phosphorylation system during steady-state hypoxia in the dog brain. Journal of Applied Physiology, 68, 2527–2535.Google Scholar
Olvera, R. L., Caetano, S. C., Stanley, J. A., Chen, H. H., Nicoletti, M., Hatch, J. P., et al. (2010). Reduced medial prefrontal N-acetyl-aspartate levels in pediatric major depressive disorder: A multi-voxel in vivo(1)H spectroscopy study. Psychiatry Research, 184, 71–76.Google Scholar
Oscar-Berman, M. (1990). Learning and memory deficits in detoxified alcoholics. NIDA Research Monographs, 101, 136–155.Google Scholar
Oscar-Berman, M. (2000). Neuropsychological vulnerabilities in chronic alcoholism. In Noronha Eckardt, A. M. & Warren, K. (Eds.), Review of NIAAA's Neuroscience and Behavioral Research Portfolio (NIAAA Research Monograph No. 34, pp. 437–472). Bethesda, MD: National Institutes of Health.Google Scholar
Oscar-Berman, M., & Marinkovic, K. (2003). Alcoholism and the brain: An overview. Alcohol Research and Health, 27, 125–133.Google Scholar
Oscar-Berman, M., & Marinkovic, K. (2007). Alcohol: Effects on neurobehavioral functions and the brain. Neuropsychology Review, 17, 239–257.Google Scholar
Ozturk, A., Degaonkar, M., Matson, M. A., Wells, C. T., Mahone, E. M., & Horska, A. (2009). Proton MR spectroscopy correlates of frontal lobe function in healthy children. American Journal of Neuroradiology, 30, 1308–1314.CrossRefGoogle ScholarPubMed
Parsons, O. A., & Nixon, S. J. (1998). Cognitive functioning in sober social drinkers: A review of the research since 1986. Journal of Studies on Alcohol, 59, 180–190.Google Scholar
Patel, A. B., de Graaf, R. A., Mason, G. F., Rothman, D. L., Shulman, R. G., & Behar, K. L. (2005). The contribution of GABA to glutamate/glutamine cycling and energy metabolism in the rat cortex in vivo. Proceedings of the National Academy of Sciences, 102, 5588–5593.Google Scholar
Paulus, M. P., Tapert, S. F., Pulido, C., & Schuckit, M. A. (2006). Alcohol attenuates load-related activation during a working memory task: Relation to level of response to alcohol. Alcoholism: Clinical and Experimental Research, 30, 1363–1371.Google Scholar
Paus, T., Keshavan, M., & Giedd, J. N. (2008). Why do many psychiatric disorders emerge during adolescence? Nature Reviews Neuroscience, 9, 947–957.Google Scholar
Petroff, O. A., Mattson, R. H., & Rothman, D. L. (2000). Proton MRS: GABA and glutamate. Advances in Neurology, 83, 261–271.Google Scholar
Pettegrew, J. W., Keshavan, M. S., Panchalingam, K., Strychor, S., Kaplan, D. B., Tretta, M. G., et al. (1991). Alterations in brain high-energy phosphate and membrane phospholipid metabolism in first-episode, drug-naive schizophrenics: A pilot study of the dorsal prefrontal cortex by in vivo phosphorus 31 nuclear magnetic resonance spectroscopy. Archives of General Psychiatry, 48, 563–568.Google Scholar
Pfefferbaum, A., Adalsteinsson, E., Spielman, D., Sullivan, E. V., & Lim, K. O. (1999). In vivo brain concentrations of N-acetyl compounds, creatine, and choline in Alzheimer disease. Archives of General Psychiatry, 56, 185–192.Google Scholar
Pfefferbaum, A., Sullivan, E. V., Mathalon, D. H., & Lim, K. O. (1997). Frontal lobe volume loss observed with magnetic resonance imaging in older chronic alcoholics. Alcoholism: Clinical and Experimental Research, 21, 521–529.CrossRefGoogle ScholarPubMed
Pfleiderer, B., Ohrmann, P., Suslow, T., Wolgast, M., Gerlach, A. L., Heindel, W., et al. (2004). N-acetylaspartate levels of left frontal cortex are associated with verbal intelligence in women but not in men: A proton magnetic resonance spectroscopy study. Neuroscience, 123, 1053–1058.CrossRefGoogle ScholarPubMed
Pouwels, P. J., Brockmann, K., Kruse, B., Wilken, B., Wick, M., Hanefeld, F., et al. (1999). Regional age dependence of human brain metabolites from infancy to adulthood as detected by quantitative localized proton MRS. Pediatric Research, 46, 474–485.Google Scholar
Pouwels, P. J., & Frahm, J. (1997). Differential distribution of NAA and NAAG in human brain as determined by quantitative localized proton MRS. NMR in Biomedicine, 10, 73–78.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Pouwels, P. J., & Frahm, J. (1998). Regional metabolite concentrations in human brain as determined by quantitative localized proton MRS. Magnetic Resonance in Medicine, 39, 53–60.Google Scholar
Provencher, S. W. (1993). Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magnetic Resonance in Medicine, 30, 672–679.Google Scholar
Provencher, S. W. (2001). Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR in Biomedicine, 14, 260–264.Google Scholar
Purdon, S. E., Valiakalayil, A., Hanstock, C. C., Seres, P., & Tibbo, P. (2008). Elevated 3T proton MRS glutamate levels associated with poor Continuous Performance Test (CPT-0X) scores and genetic risk for schizophrenia. Schizophrenia Research, 99, 218–224.Google Scholar
Raininko, R., & Mattsson, P. (2010). Metabolite concentrations in supraventricular white matter from teenage to early old age: A short echo time 1H magnetic resonance spectroscopy (MRS) study. Acta Radiologica, 51, 309–315.Google Scholar
Ross, A. J., Sachdev, P. S., Wen, W., Valenzuela, M. J., & Brodaty, H. (2005). Cognitive correlates of 1H MRS measures in the healthy elderly brain. Brain Research Bulletin, 66, 9–16.Google Scholar
Rubia, K., Smith, A. B., Taylor, E., & Brammer, M. (2007). Linear age-correlated functional development of right inferior fronto–striatal–cerebellar networks during response inhibition and anterior cingulate during error-related processes. Human Brain Mapping, 28, 1163–1177.Google Scholar
Rubia, K., Smith, A. B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., et al. (2006). Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Human Brain Mapping, 27, 973–993.Google Scholar
SAMHSA. (2004). Results from the 2003 National Survey on Drug Use and Health: National findings (Office of Applied Studies, NSDUH Series H-25, DHHS Publication No. SMA 04-3964). Washington, DC: Author.Google Scholar
Scherf, K. S., Sweeney, J. A., & Luna, B. (2006). Brain basis of developmental change in visuospatial working memory. Journal of Cognitive Neuroscience, 18, 1045–1058.Google Scholar
Schmithorst, V. J., Wilke, M., Dardzinski, B. J., & Holland, S. K. (2002). Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: A cross-sectional diffusion-tensor MR imaging study. Radiology, 222, 212–218.Google Scholar
Schweinsburg, A. D., McQueeny, T., Nagel, B. J., Eyler, L. T., & Tapert, S. F. (2010). A preliminary study of functional magnetic resonance imaging response during verbal encoding among adolescent binge drinkers. Alcohol, 44, 111–117.Google Scholar
Shulman, R. G., Rothman, D. L., Behar, K. L., & Hyder, F. (2004). Energetic basis of brain activity: Implications for neuroimaging. Trends in Neurosciences, 27, 489–495.CrossRefGoogle ScholarPubMed
Sikoglu, E. M., Jensen, J. E., Vitaliano, G., Liso Navarro, A. A., Renshaw, P. F., Frazier, J. A., et al. (2013). Bioenergetic measurements in children with bipolar disorder: A pilot 31P magnetic resonance spectroscopy study. PLoS One, 8, e54536.Google Scholar
Silveri, M. M., Crowley, D. J., Covell, M. J., Acharya, D., Sneider, J. T., Rosso, I. M., et al. (2013). Frontal lobe GABA levels during adolescence: Associations with impulsivity and response inhibition. Biological Psychiatry, 74, 296–304.Google Scholar
Silveri, M. M., Rogowska, J., McCaffrey, A., & Yurgelun-Todd, D. A. (2011). Adolescents at risk for alcohol abuse demonstrate altered frontal lobe activation during stroop performance. Alcoholism: Clinical and Experimental Research, 35, 218–228.Google Scholar
Silveri, M. M., & Spear, L. P. (2004). The effects of NMDA and GABAA pharmacological manipulations on acute and rapid tolerance to ethanol during ontogeny. Alcoholism: Clinical and Experimental Research, 28, 884–894.Google Scholar
Soliva, J. C., Moreno, A., Fauquet, J., Bielsa, A., Carmona, S., Gispert, J. D., et al. (2010). Cerebellar neurometabolite abnormalities in pediatric attention/deficit hyperactivity disorder: A proton MR spectroscopic study. Neuroscience Letters, 470, 60–64.Google Scholar
Somerville, L. H., Jones, R. M., & Casey, B. J. (2010). A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain and Cognition, 72, 124–133.Google Scholar
Sowell, E. R., Thompson, P. M., Holmes, C. J., Jernigan, T. L., & Toga, A. W. (1999). In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nature Neuroscience, 2, 859–861.Google Scholar
Sowell, E. R., Trauner, D. A., Gamst, A., & Jernigan, T. L. (2002). Development of cortical and subcortical brain structures in childhood and adolescence: A structural MRI study. Developmental Medicine and Child Neurology, 44, 4–16.Google Scholar
Spadoni, A. D., Norman, A. L., Schweinsburg, A. D., & Tapert, S. F. (2008). Effects of family history of alcohol use disorders on spatial working memory BOLD response in adolescents. Alcoholism: Clinical and Experimental Research, 32, 1135–1145.Google Scholar
Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417–463.Google Scholar
Squeglia, L. M., Schweinsburg, A. D., Pulido, C., & Tapert, S. F. (2011). Adolescent binge drinking linked to abnormal spatial working memory brain activation: Differential gender effects. Alcoholism: Clinical and Experimental Research, 35, 1831–1841.Google Scholar
Steinberg, L. (2005). Cognitive and affective development in adolescence. Trends in Cognitive Sciences, 9, 69–74.Google Scholar
Steinberg, L. (2010). A behavioral scientist looks at the science of adolescent brain development. Brain and Cognition, 72, 160–164.Google Scholar
Strawn, J. R., Chu, W. J., Whitsel, R. M., Weber, W. A., Norris, M. M., Adler, C. M., et al. (2013). A pilot study of anterior cingulate cortex neurochemistry in adolescents with generalized anxiety disorder. Neuropsychobiology, 67, 224–229.Google Scholar
Sullivan, E. V., Adalsteinsson, E., Hedehus, M., Ju, C., Moseley, M., Lim, K. O., et al. (2001). Equivalent disruption of regional white matter microstructure in ageing healthy men and women. NeuroReport, 12, 99–104.Google Scholar
Sullivan, E. V., & Pfefferbaum, A. (2005). Neurocircuitry in alcoholism: A substrate of disruption and repair. Psychopharmacology (Berlin), 180, 583–594.Google Scholar
Sumner, P., Edden, R. A. E., Bompas, A., Evans, C. J., & Singh, K. D. (2010). More GABA, less distraction: A neurochemical predictor of motor decision speed. Nature Neuroscience, 13, 825–827.Google Scholar
Tapert, S. F., Brown, G. G., Kindermann, S. S., Cheung, E. H., Frank, L. R., & Brown, S. A. (2001). fMRI measurement of brain dysfunction in alcohol-dependent young women. Alcoholism: Clinical and Experimental Research, 25, 236–245.Google Scholar
Tapert, S. F., Pulido, C., Paulus, M. P., Schuckit, M. A., & Burke, C. (2004). Level of response to alcohol and brain response during visual working memory. Journal of Studies on Alcohol and Drugs, 65, 692–700.Google Scholar
Tapert, S. F., Schweinsburg, A. D., Barlett, V. C., Brown, S. A., Frank, L. R., Brown, G. G., et al. (2004). Blood oxygen level dependent response and spatial working memory in adolescents with alcohol use disorders. Alcoholism: Clinical and Experimental Research, 28, 1577–1586.Google Scholar
Tkac, I., Andersen, P., Adriany, G., Merkle, H., Ugurbil, K., & Gruetter, R. (2001). In vivo 1H NMR spectroscopy of the human brain at 7 T. Magnetic Resonance in Medicine, 46, 451–456.Google Scholar
Tkac, I., Oz, G., Adriany, G., Ugurbil, K., & Gruetter, R. (2009). In vivo 1H NMR spectroscopy of the human brain at high magnetic fields: Metabolite quantification at 4T vs. 7T. Magnetic Resonance in Medicine, 62, 868–879.Google Scholar
Toft, P. B., Christiansen, P., Pryds, O., Lou, H. C., & Henriksen, O. (1994). T1, T2, and concentrations of brain metabolites in neonates and adolescents estimated with H-1 MR spectroscopy. Journal of Magnetic Resonance Imaging, 4, 1–5.Google Scholar
Toga, A. W., Thompson, P. M., & Sowell, E. R. (2006). Mapping brain maturation. Trends in Neurosciences, 29, 148–159.Google Scholar
Tsai, G., & Coyle, J. T. (1998). The role of glutamatergic neurotransmission in the pathophysiology of alcoholism. Annual Review of Medicine, 49, 173–184.Google Scholar
Valenzuela, M. J., Sachdev, P. S., Wen, W., Shnier, R., Brodaty, H., & Gillies, D. (2000). Dual voxel proton magnetic resonance spectroscopy in the healthy elderly: Subcortical-frontal axonal N-acetylaspartate levels are correlated with fluid cognitive abilities independent of structural brain changes. NeuroImage, 12, 747–756.Google Scholar
van der Knaap, M. S., van der Grond, J., van Rijen, P. C., Faber, J. A., Valk, J., & Willemse, K. (1990). Age-dependent changes in localized proton and phosphorus MR spectroscopy of the brain. Radiology, 176, 509–515.Google Scholar
Van Leijenhorst, L., Zanolie, K., Van Meel, C. S., Westenberg, P. M., Rombouts, S. A. R. B., & Crone, E. A. (2011). What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cerebral Cortex, 20, 61–69.Google Scholar
Volz, H. P., Hübner, G., Rzanny, R., Rößger, G., Preußler, B., Eichhorn, M., et al. (1998). High-energy phosphates in the frontal lobe correlate with Wisconsin Card Sort Test performance in controls, not in schizophrenics: A 31phosphorus magnetic resonance spectroscopic and neuropsychological investigation. Schizophrenia Research, 31, 37–47.Google Scholar
Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K., & Eppenberger, H. M. (1992). Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: The “phosphocreatine circuit” for cellular energy homeostasis. Biochemical Journal, 281(Pt. 1), 21–40.Google Scholar
Weber, O. M., Trabesinger, A. H., Duc, C. O., Meier, D., & Boesiger, P. (1997). Detection of hidden metabolites by localized proton magnetic resonance spectroscopy in vivo. Technology and Health Care, 5, 471–491.Google Scholar
Whiteside, S. P., Abramowitz, J. S., & Port, J. D. (2012). Decreased caudate N-acetyl-l-aspartic acid in pediatric obsessive–compulsive disorder and the effects of behavior therapy. Psychiatry Research, 202, 53–59.Google Scholar
Wiedermann, D., Schuff, N., Matson, G. B., Soher, B. J., Du, A. T., Maudsley, A. A., et al. (2001). Short echo time multislice proton magnetic resonance spectroscopic imaging in human brain: Metabolite distributions and reliability. Magnetic Resonance Imaging, 19, 1073–1080.Google Scholar
Wolfson, M., Bersudsky, Y., Hertz, E., Berkin, V., Zinger, E., & Hertz, L. (2000). A model of inositol compartmentation in astrocytes based upon efflux kinetics and slow inositol depletion after uptake inhibition. Neurochemical Research, 25, 977–982.Google Scholar
Yakovlev, P. I., & Lecours, A. R. (1967). The myelogenetic cycles of regional maturation of the brain. In Regional development of the brain in early life (pp. 3–70). Oxford: Blackwell Scientific.Google Scholar
Yeo, R. A., Hill, D., Campbell, R., Vigil, J., & Brooks, W. M. (2000). Developmental instability and working memory ability in children: A magnetic resonance spectroscopy investigation. Developmental Neuropsychology, 17, 143–159.Google Scholar