The Effect of Perinatal Brain Injury on Dopaminergic Function and Hippocampal Volume in Adult Life

Overview

Journal Elife

Specialty Biology

Date 2017 Nov 29

PMID 29179814

Citations 19

Authors

Sean Froudist-Walsh

Michael Ap Bloomfield

Mattia Veronese

Jasmin Kroll

Vyacheslav R Karolis

Sameer Jauhar

Ilaria Bonoldi

Philip K McGuire

Shitij Kapur

Robin M Murray

Chiara Nosarti

Oliver Howes

Affiliations

Soon will be listed here.

Abstract

Perinatal brain injuries, including hippocampal lesions, cause lasting changes in dopamine function in rodents, but it is not known if this occurs in humans. We compared adults who were born very preterm with perinatal brain injury to those born very preterm without perinatal brain injury, and age-matched controls born at full term using [18F]-DOPA PET and structural MRI. Dopamine synthesis capacity was reduced in the perinatal brain injury group relative to those without brain injury (Cohen's = 1.36, p=0.02) and the control group (Cohen's = 1.07, p=0.01). Hippocampal volume was reduced in the perinatal brain injury group relative to controls (Cohen's = 1.17, p=0.01) and was positively correlated with striatal dopamine synthesis capacity (r = 0.344, p=0.03). This is the first evidence in humans linking neonatal hippocampal injury to adult dopamine dysfunction, and provides a potential mechanism linking early life risk factors to adult mental illness.

Citing Articles

Polysomnographically Defined Restless Sleep Disorder and Periodic Limb Movements during Sleep in Children Born Prematurely.

DelRosso L, Artinian H, Mogavero M, Bruni O, Witmans M, Tablizo M Children (Basel). 2024; 11(6).

PMID: 38929237 PMC: 11202265. DOI: 10.3390/children11060658.

Dopamine signaling enriched striatal gene set predicts striatal dopamine synthesis and physiological activity in vivo.

Sportelli L, Eisenberg D, Passiatore R, DAmbrosio E, Antonucci L, Bettina J Nat Commun. 2024; 15(1):3342.

PMID: 38688917 PMC: 11061310. DOI: 10.1038/s41467-024-47456-5.

Indirect evidence for altered dopaminergic neurotransmission in very premature-born adults.

Schinz D, Schmitz-Koep B, Zimmermann J, Brandes E, Tahedl M, Menegaux A Hum Brain Mapp. 2023; 44(15):5125-5138.

PMID: 37608591 PMC: 10502650. DOI: 10.1002/hbm.26451.

Mechanisms of Tertiary Neurodegeneration after Neonatal Hypoxic-Ischemic Brain Damage.

Levison S, Rocha-Ferreira E, Kim B, Hagberg H, Fleiss B, Gressens P Pediatr Med. 2023; 5.

PMID: 37601279 PMC: 10438849. DOI: 10.21037/pm-20-104.

A polygenic score indexing a DRD2-related co-expression network is associated with striatal dopamine function.

DAmbrosio E, Pergola G, Pardinas A, Dahoun T, Veronese M, Sportelli L Sci Rep. 2022; 12(1):12610.

PMID: 35871219 PMC: 9308811. DOI: 10.1038/s41598-022-16442-6.

References

Nicodemus K, Marenco S, Batten A, Vakkalanka R, Egan M, Straub R . Serious obstetric complications interact with hypoxia-regulated/vascular-expression genes to influence schizophrenia risk. Mol Psychiatry. 2008; 13(9):873-7. DOI: 10.1038/sj.mp.4002153. View

Schultz W, Dayan P, Montague P . A neural substrate of prediction and reward. Science. 1997; 275(5306):1593-9. DOI: 10.1126/science.275.5306.1593. View

Ashok A, Mizuno Y, Volkow N, Howes O . Association of Stimulant Use With Dopaminergic Alterations in Users of Cocaine, Amphetamine, or Methamphetamine: A Systematic Review and Meta-analysis. JAMA Psychiatry. 2017; 74(5):511-519. PMC: 5419581. DOI: 10.1001/jamapsychiatry.2017.0135. View

Howes O, McCutcheon R, Owen M, Murray R . The Role of Genes, Stress, and Dopamine in the Development of Schizophrenia. Biol Psychiatry. 2016; 81(1):9-20. PMC: 5675052. DOI: 10.1016/j.biopsych.2016.07.014. View

Jenkinson M, Bannister P, Brady M, Smith S . Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002; 17(2):825-41. DOI: 10.1016/s1053-8119(02)91132-8. View

Ross G, Boatright S, AULD P, Nass R . Specific cognitive abilities in 2-year-old children with subependymal and mild intraventricular hemorrhage. Brain Cogn. 1996; 32(1):1-13. DOI: 10.1006/brcg.1996.0054. View

Cachope R, Cheer J . Local control of striatal dopamine release. Front Behav Neurosci. 2014; 8:188. PMC: 4033078. DOI: 10.3389/fnbeh.2014.00188. View

Vollmer B, Roth S, Baudin J, Stewart A, Neville B, Wyatt J . Predictors of long-term outcome in very preterm infants: gestational age versus neonatal cranial ultrasound. Pediatrics. 2003; 112(5):1108-14. DOI: 10.1542/peds.112.5.1108. View

Nosarti C, Walshe M, Rushe T, Rifkin L, Wyatt J, Murray R . Neonatal ultrasound results following very preterm birth predict adolescent behavioral and cognitive outcome. Dev Neuropsychol. 2011; 36(1):118-35. DOI: 10.1080/87565641.2011.540546. View

10.

Studholme C, Hill D, Hawkes D . Automated 3-D registration of MR and CT images of the head. Med Image Anal. 1996; 1(2):163-75. DOI: 10.1016/s1361-8415(96)80011-9. View

11.

Froudist-Walsh S, Karolis V, Caldinelli C, Brittain P, Kroll J, Rodriguez-Toscano E . Very Early Brain Damage Leads to Remodeling of the Working Memory System in Adulthood: A Combined fMRI/Tractography Study. J Neurosci. 2015; 35(48):15787-99. PMC: 4666909. DOI: 10.1523/JNEUROSCI.4769-14.2015. View

12.

Howes O, Bose S, Turkheimer F, Valli I, Egerton A, Valmaggia L . Dopamine synthesis capacity before onset of psychosis: a prospective [18F]-DOPA PET imaging study. Am J Psychiatry. 2011; 168(12):1311-7. PMC: 3682447. DOI: 10.1176/appi.ajp.2011.11010160. View

13.

Huang B, Castillo M . Hypoxic-ischemic brain injury: imaging findings from birth to adulthood. Radiographics. 2008; 28(2):417-39. DOI: 10.1148/rg.282075066. View

14.

Calabresi P, Picconi B, Tozzi A, Di Filippo M . Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci. 2007; 30(5):211-9. DOI: 10.1016/j.tins.2007.03.001. View

15.

Lipska B, Weinberger D . To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology. 2000; 23(3):223-39. DOI: 10.1016/S0893-133X(00)00137-8. View

16.

PATLAK C, Blasberg R . Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J Cereb Blood Flow Metab. 1985; 5(4):584-90. DOI: 10.1038/jcbfm.1985.87. View

17.

Kumakura Y, Cumming P . PET studies of cerebral levodopa metabolism: a review of clinical findings and modeling approaches. Neuroscientist. 2009; 15(6):635-50. DOI: 10.1177/1073858409338217. View

18.

Floresco S, Todd C, Grace A . Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J Neurosci. 2001; 21(13):4915-22. PMC: 6762358. View

19.

Williams G, Goldman-Rakic P . Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature. 1995; 376(6541):572-5. DOI: 10.1038/376572a0. View

20.

Fischl B, Salat D, Busa E, Albert M, Dieterich M, Haselgrove C . Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002; 33(3):341-55. DOI: 10.1016/s0896-6273(02)00569-x. View