Making Dopamine Connections in Adolescence

Overview

Journal Trends Neurosci

Specialty Neurology

Date 2017 Oct 17

PMID 29032842

Citations 62

Authors

Daniel Hoops

Cecilia Flores

Affiliations

Soon will be listed here.

Abstract

A dramatic maturational process ongoing in adolescence is prefrontal cortex development, including its dopamine innervation. Dopamine axons grow from the striatum to the prefrontal cortex, the only known case of long-distance axon growth during adolescence. This is coordinated by the Netrin-1 guidance cue receptor DCC (deleted in colorectal cancer), which in turn controls the intrinsic development of the prefrontal cortex itself. Stimulant drugs in adolescence alter DCC in dopamine neurons and, in turn prefrontal cortex maturation, impacting cognitive abilities. Variations in DCC expression are linked to psychiatric conditions of prefrontal cortex dysfunction, and microRNA regulation of DCC may be key to determining adolescent vulnerability or resilience. Since early interventions are proving to effectively ameliorate disease outcome, the Netrin-1 system is a promising therapeutic target.

Citing Articles

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References

Smiley J, Goldman-Rakic P . Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique. Cereb Cortex. 1993; 3(3):223-38. DOI: 10.1093/cercor/3.3.223. View

Rosenberg D, Lewis D . Changes in the dopaminergic innervation of monkey prefrontal cortex during late postnatal development: a tyrosine hydroxylase immunohistochemical study. Biol Psychiatry. 1994; 36(4):272-7. DOI: 10.1016/0006-3223(94)90610-6. View

Leday G, Vertes P, Richardson S, Greene J, Regan T, Khan S . Replicable and Coupled Changes in Innate and Adaptive Immune Gene Expression in Two Case-Control Studies of Blood Microarrays in Major Depressive Disorder. Biol Psychiatry. 2017; 83(1):70-80. PMC: 5720346. DOI: 10.1016/j.biopsych.2017.01.021. View

Manitt C, Mimee A, Eng C, Pokinko M, Stroh T, Cooper H . The netrin receptor DCC is required in the pubertal organization of mesocortical dopamine circuitry. J Neurosci. 2011; 31(23):8381-94. PMC: 6623341. DOI: 10.1523/JNEUROSCI.0606-11.2011. View

Varadarajan S, Kong J, Phan K, Kao T, Panaitof S, Cardin J . Netrin1 Produced by Neural Progenitors, Not Floor Plate Cells, Is Required for Axon Guidance in the Spinal Cord. Neuron. 2017; 94(4):790-799.e3. PMC: 5576449. DOI: 10.1016/j.neuron.2017.03.007. View

Grant A, Hoops D, Labelle-Dumais C, Prevost M, Rajabi H, Kolb B . Netrin-1 receptor-deficient mice show enhanced mesocortical dopamine transmission and blunted behavioural responses to amphetamine. Eur J Neurosci. 2007; 26(11):3215-28. DOI: 10.1111/j.1460-9568.2007.05888.x. View

Sesack S, Hawrylak V, Melchitzky D, Lewis D . Dopamine innervation of a subclass of local circuit neurons in monkey prefrontal cortex: ultrastructural analysis of tyrosine hydroxylase and parvalbumin immunoreactive structures. Cereb Cortex. 1998; 8(7):614-22. DOI: 10.1093/cercor/8.7.614. View

Lopez J, Lim R, Cruceanu C, Crapper L, Fasano C, Labonte B . miR-1202 is a primate-specific and brain-enriched microRNA involved in major depression and antidepressant treatment. Nat Med. 2014; 20(7):764-8. PMC: 4087015. DOI: 10.1038/nm.3582. View

Benes F, Taylor J, Cunningham M . Convergence and plasticity of monoaminergic systems in the medial prefrontal cortex during the postnatal period: implications for the development of psychopathology. Cereb Cortex. 2000; 10(10):1014-27. DOI: 10.1093/cercor/10.10.1014. View

10.

Berger B, Gaspar P, Verney C . Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci. 1991; 14(1):21-7. DOI: 10.1016/0166-2236(91)90179-x. View

11.

Floresco S . Prefrontal dopamine and behavioral flexibility: shifting from an "inverted-U" toward a family of functions. Front Neurosci. 2013; 7:62. PMC: 3630325. DOI: 10.3389/fnins.2013.00062. View

12.

Ventura R, Alcaro A, Cabib S, Conversi D, Mandolesi L, Puglisi-Allegra S . Dopamine in the medial prefrontal cortex controls genotype-dependent effects of amphetamine on mesoaccumbens dopamine release and locomotion. Neuropsychopharmacology. 2003; 29(1):72-80. DOI: 10.1038/sj.npp.1300300. View

13.

Yamamuro K, Yoshino H, Ogawa Y, Makinodan M, Toritsuka M, Yamashita M . Social Isolation During the Critical Period Reduces Synaptic and Intrinsic Excitability of a Subtype of Pyramidal Cell in Mouse Prefrontal Cortex. Cereb Cortex. 2017; 28(3):998-1010. DOI: 10.1093/cercor/bhx010. View

14.

Flores C, Manitt C, Rodaros D, Thompson K, Rajabi H, Luk K . Netrin receptor deficient mice exhibit functional reorganization of dopaminergic systems and do not sensitize to amphetamine. Mol Psychiatry. 2004; 10(6):606-12. DOI: 10.1038/sj.mp.4001607. View

15.

Jamuar S, Schmitz-Abe K, DGama A, Drottar M, Chan W, Peeva M . Biallelic mutations in human DCC cause developmental split-brain syndrome. Nat Genet. 2017; 49(4):606-612. PMC: 5374027. DOI: 10.1038/ng.3804. View

16.

. Age limits and adolescents. Paediatr Child Health. 2009; 8(9):577-8. PMC: 2794325. DOI: 10.1093/pch/8.9.577. View

17.

Marsh A, Heron D, Edwards T, Quartier A, Galea C, Nava C . Mutations in DCC cause isolated agenesis of the corpus callosum with incomplete penetrance. Nat Genet. 2017; 49(4):511-514. PMC: 5894478. DOI: 10.1038/ng.3794. View

18.

Manitt C, Kennedy T . Where the rubber meets the road: netrin expression and function in developing and adult nervous systems. Prog Brain Res. 2002; 137:425-42. DOI: 10.1016/s0079-6123(02)37034-1. View

19.

Makinodan M, Rosen K, Ito S, Corfas G . A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science. 2012; 337(6100):1357-60. PMC: 4165613. DOI: 10.1126/science.1220845. View

20.

Wahid F, Shehzad A, Khan T, Kim Y . MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochim Biophys Acta. 2010; 1803(11):1231-43. DOI: 10.1016/j.bbamcr.2010.06.013. View