Abstract
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.
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Acknowledgments
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).
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All authors declare that they have no conflicts of interest.
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T. Gleich and R. C. Lorenz have contributed equally to the manuscript.
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Gleich, T., Lorenz, R.C., Pöhland, L. et al. Frontal glutamate and reward processing in adolescence and adulthood. Brain Struct Funct 220, 3087–3099 (2015). https://doi.org/10.1007/s00429-014-0844-3
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DOI: https://doi.org/10.1007/s00429-014-0844-3