Frontal glutamate and reward processing in adolescence and adulthood
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The fronto-limbic network interaction, driven by glutamatergic and dopaminergic neurotransmission, represents a core mechanism of motivated behavior and personality traits. Reward seeking behavior undergoes tremendous changes in adolescence paralleled by neurobiological changes of this network including the prefrontal cortex, striatum and amygdala. Since fronto-limbic dysfunctions also underlie major psychiatric diseases beginning in adolescence, this investigation focuses on network characteristics separating adolescents from adults. To investigate differences in network interactions, the brain reward system activity (slot machine task) together with frontal glutamate concentration (anterior cingulate cortex, ACC) was measured in 28 adolescents and 26 adults employing functional magnetic resonance imaging and magnetic resonance spectroscopy, respectively. An inverse coupling of glutamate concentrations in the ACC and activation of the ventral striatum was observed in adolescents. Further, amygdala response in adolescents was negatively correlated with the personality trait impulsivity. For adults, no significant associations of network components or correlations with impulsivity were found. The inverse association between frontal glutamate concentration and striatal activation in adolescents is in line with the triadic model of motivated behavior stressing the important role of frontal top–down inhibition on limbic structures. Our data identified glutamate as the mediating neurotransmitter of this inhibitory process and demonstrates the relevance of glutamate on the reward system and related behavioral traits like impulsivity. This fronto-limbic coupling may represent a vulnerability factor for psychiatric disorders starting in adolescence but not in adulthood.
KeywordsReward processing Aging Adolescence fMRI Ventral striatum Glutamate MRS
We thank Julia Frenzel, Lucas Adam, Sa Luo, Sabrina Golde, Charlotte Klein and Eva Flemming for help with data acquisition. This study was supported by the German Ministry for Education and Research (BMBF 01GQ0914), the Volkswagen Foundation (Schumpeter Fellowship, II/84 452), the German National Academic Foundation grant to RCL, and by the German Research Foundation (DFG GA707/6-1).
Conflict of interest
All authors declare that they have no conflicts of interest.
- Hoerst M, Weber-Fahr W, Tunc-Skarka N et al (2010) Correlation of glutamate levels in the anterior cingulate cortex with self-reported impulsivity in patients with borderline personality disorder and healthy controls. Arch Gen Psychiatry 67:946–954. doi: 10.1001/archgenpsychiatry.2010.93 CrossRefPubMedGoogle Scholar
- Labudda K, Mertens M, Steinkroeger C et al (2014) Lesion side matters––an fMRI study on the association between neural correlates of watching dynamic fearful faces and their evaluation in patients with temporal lobe epilepsy. Epilepsy Behav 31:321–328. doi: 10.1016/j.yebeh.2013.10.014 CrossRefPubMedGoogle Scholar
- Mon A, Durazzo TC, Meyerhoff DJ (2012) Glutamate, GABA, and other cortical metabolite concentrations during early abstinence from alcohol and their associations with neurocognitive changes. Drug Alcohol Depend 125:27–36. doi: 10.1016/j.drugalcdep.2012.03.012 PubMedCentralCrossRefPubMedGoogle Scholar
- Portella MJ, de Diego-Adeliño J, Gómez-Ansón B et al (2011) Ventromedial prefrontal spectroscopic abnormalities over the course of depression: a comparison among first episode, remitted recurrent and chronic patients. J Psychiatr Res 45:427–434. doi: 10.1016/j.jpsychires.2010.08.010 CrossRefPubMedGoogle Scholar
- Richards JM, Plate RC, Ernst M (2013) A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: the impact of task design and implications for understanding neurodevelopment. Neurosci Biobehav Rev 37:976–991. doi: 10.1016/j.neubiorev.2013.03.004 CrossRefPubMedGoogle Scholar