Association of emotional and behavioral problems with the development of the substantia nigra, subthalamic nucleus, and red nucleus volumes and asymmetries from childhood to adolescence: A longitudinal cohort study.
Journal
Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664
Informations de publication
Date de publication:
26 Feb 2024
26 Feb 2024
Historique:
received:
22
05
2023
accepted:
23
01
2024
revised:
17
01
2024
medline:
26
2
2024
pubmed:
26
2
2024
entrez:
25
2
2024
Statut:
epublish
Résumé
The substantia nigra (SN), subthalamic nucleus (STN), and red nucleus (RN) have been widely studied as important biomarkers of degenerative diseases. However, how they develop in childhood and adolescence and are affected by emotional behavior has not been studied thus far. This population-based longitudinal cohort study used data from a representative sample followed two to five times. Emotional and behavioral problems were assessed with the Strengths and Difficulties Questionnaire (SDQ). Linear mixed models were used to map developmental trajectories and behavioral regulation. Using an innovative automated image segmentation technique, we quantified the volumes and asymmetries of the SN, STN and RN with 1226 MRI scans of a large longitudinal sample of 667 subjects aged 6-15 years and mapped their developmental trajectories. The results showed that the absolute and relative volumes of the bilateral SN and right STN showed linear increases, while the absolute volume of the right RN and relative volume of the bilateral RN decreased linearly, these effects were not affected by gender. Hyperactivity/inattention weakened the increase in SN volume and reduced the absolute volume of the STN, conduct problems impeded the RN volume from decreasing, and emotional symptoms changed the direction of SN lateralization. This longitudinal cohort study mapped the developmental trajectories of SN, STN, and RN volumes and asymmetries from childhood to adolescence, and found the association of emotional symptoms, conduct problems, and hyperactivity/inattention with these trajectories, providing guidance for preventing and intervening in cognitive and emotional behavioral problems.
Identifiants
pubmed: 38403656
doi: 10.1038/s41398-024-02803-4
pii: 10.1038/s41398-024-02803-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
117Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 32200873
Informations de copyright
© 2024. The Author(s).
Références
de Hollander G, Keuken MC, van der Zwaag W, Forstmann BU, Trampel R. Comparing functional MRI protocols for small, iron-rich basal ganglia nuclei such as the subthalamic nucleus at 7 T and 3 T. Hum Brain Mapp. 2017;38:3226–48.
pubmed: 28345164
pmcid: 6867009
Sonne J, Reddy V, Beato MR Neuroanatomy, Substantia Nigra. StatPearls. StatPearls Publishing, 2021.
Smith ID, Grace AA. Role of the subthalamic nucleus in the regulation of nigral dopamine neuron activity. Synapse. 1992;12:287–303.
pubmed: 1465742
Philippens IHCHM, Wubben JA, Franke SK, Hofman S, Langermans JAM. Involvement of the red nucleus in the compensation of Parkinsonism may explain why primates can develop Stable Parkinson’s Disease. Sci Rep. 2019;9:880.
pubmed: 30696912
pmcid: 6351580
Langley J, Hussain S, Flores JJ, Bennett IJ, Hu X. Characterization of age-related microstructural changes in locus coeruleus and substantia nigra pars compacta. Neurobiol Aging. 2020;87:89–97.
pubmed: 31870645
Cao CY, Pan YX, Li DY, Zhan SK, Zhang J, Sun BM. Subthalamus deep brain stimulation for primary dystonia patients: a long-term follow-up study. Mov Disord. 2013;28:1877–82.
pubmed: 23861342
van Horne CG, Quintero JE, Slevin JT, Anderson-Mooney A, Gurwell JA, Welleford AS, et al. Peripheral nerve grafts implanted into the substantia nigra in patients with Parkinson’s disease during deep brain stimulation surgery: 1-year follow-up study of safety, feasibility, and clinical outcome. J Neurosurg. 2018;129:1550–61.
pubmed: 29451447
Tomasi D, Volkow ND. Functional connectivity of substantia nigra and ventral tegmental area: maturation during adolescence and effects of ADHD. Cereb Cortex. 2014;24:935–44.
pubmed: 23242198
Tan L, Ge H, Tang J, Fu C, Duanmu W, Chen Y, et al. Amantadine preserves dopamine level and attenuates depression-like behavior induced by traumatic brain injury in rats. Behav Brain Res. 2015;279:274–82.
pubmed: 25447294
Gao L, Xue Q, Gong S, Li G, Tong W, Fan M, et al. Structural and functional alterations of substantia nigra and associations with anxiety and depressive symptoms following traumatic brain injury. Front Neurol. 2022;13:719778.
pubmed: 35449518
pmcid: 9017679
Hirsch EC, Mouatt A, Faucheux B, Bonnet AM, Agid Y. Dopamine, tremor, and Parkinson’s disease. Lancet. 1992;340:125–6.
pubmed: 1352004
Manjon JV, Berto A, Romero JE, Lanuza E, Vivo-Hernando R, Aparici-Robles F, et al. pBrain: A novel pipeline for Parkinson related brain structure segmentation. NeuroImage Clin. 2020;25:102184.
pubmed: 31982678
pmcid: 6992999
Iova A, Garmashov A, Androuchtchenko N, Kehrer M, Berg D, Becker G, et al. Postnatal decrease in substantia nigra echogenicity - Implications for the pathogenesis of Parkinson’s disease. J Neurol. 2004;251:1451–4.
pubmed: 15645343
Romanos M, Weise D, Schliesser M, Schecklmann M, Loffler J, Warnke A, et al. Structural abnormality of the substantia nigra in children with attention-deficit hyperactivity disorder. J psychiatry Neurosci : JPN. 2010;35:55–58.
pubmed: 20040247
pmcid: 2799505
Krauel K, Feldhaus HC, Simon A, Rehe C, Glaser M, Flechtner HH, et al. Increased echogenicity of the substantia nigra in children and adolescents with attention-deficit/hyperactivity disorder. Biol Psychiatry. 2010;68:352–8.
pubmed: 20227683
Sepehrmanesh Z, Asayeshi A, Kakhki RD, Assarian F, Rahimi H, Arani SRM. Echogenicity and size of substantia nigra on transcranial sonography (TCS) in patients with attention-deficit/hyperactivity disorder and healthy children aged 6-12 years: a comparative study. Egypt J Neurol Psychiatry Neurosurg. 2023;59:1–7.
Elliott BL, D’Ardenne K, Mukherjee P, Schweitzer JB, McClure SM. Limbic and executive meso- and nigrostriatal tracts predict impulsivity differences in attention-deficit/hyperactivity disorder. Biol Psychiatry Cogn Neurosci Neuroimaging. 2022;7:415–23.
pubmed: 34051394
Lambert C, Zrinzo L, Nagy Z, Lutti A, Hariz M, Foltynie T, et al. Confirmation of functional zones within the human subthalamic nucleus: Patterns of connectivity and sub-parcellation using diffusion weighted imaging. Neuroimage. 2012;60:83–94.
pubmed: 22173294
de Hollander G, Keuken MC, Forstmann BU. The subcortical cocktail problem; mixed signals from the subthalamic nucleus and substantia nigra. PLoS One. 2015;10:e0120572.
pubmed: 25793883
pmcid: 4368736
Duann JR, Ide JS, Luo X, Li CS. Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. J Neurosci : Off J Soc Neurosci. 2009;29:10171–9.
Beauregard M, Levesque J. Functional magnetic resonance imaging investigation of the effects of neurofeedback training on the neural bases of selective attention and response inhibition in children with attention-deficit/hyperactivity disorder. Appl Psychophysiol Biofeedback. 2006;31:3–20.
pubmed: 16552626
Yu Y, FitzGerald TH, Friston KJ. Working memory and anticipatory set modulate midbrain and putamen activity. J Neurosci : Off J Soc Neurosci. 2013;33:14040–7.
Yoon JH, Minzenberg MJ, Raouf S, D’Esposito M, Carter CS. Impaired prefrontal-basal ganglia functional connectivity and substantia nigra hyperactivity in schizophrenia. Biol Psychiatry. 2013;74:122–9.
pubmed: 23290498
pmcid: 3620727
Mansfield EL, Karayanidis F, Jamadar S, Heathcote A, Forstmann BU. Adjustments of response threshold during task switching: a model-based functional magnetic resonance imaging study. J Neurosci : Off J Soc Neurosci. 2011;31:14688–92.
Espinosa-Parrilla JF, Baunez C, Apicella P. Linking reward processing to behavioral output: motor and motivational integration in the primate subthalamic nucleus. Front Comput Neurosci. 2013;7:175.
pubmed: 24381555
pmcid: 3865598
Eagle DM, Baunez C. Is there an inhibitory-response-control system in the rat? Evidence from anatomical and pharmacological studies of behavioral inhibition. Neurosci Biobehav Rev. 2010;34:50–72.
pubmed: 19615404
pmcid: 2789250
Beck AK, Lutjens G, Schwabe K, Dengler R, Krauss JK, Sandmann P. Thalamic and basal ganglia regions are involved in attentional processing of behaviorally significant events: evidence from simultaneous depth and scalp EEG. Brain Struct Funct. 2018;223:461–74.
pubmed: 28871419
Uslaner JM, Robinson TE. Subthalamic nucleus lesions increase impulsive action and decrease impulsive choice - mediation by enhanced incentive motivation? Eur J Neurosci. 2006;24:2345–54.
pubmed: 17074055
Jellinger KA. Neuropathological aspects of Alzheimer disease, Parkinson disease and frontotemporal dementia. Neurodegener Dis. 2008;5:118–21.
pubmed: 18322367
Colpan ME, Slavin KV. Subthalamic and red nucleus volumes in patients with Parkinson’s disease: Do they change with disease progression? Parkinsonism Relat Disord. 2010;16:398–403.
pubmed: 20452266
Zhong Z, Merkitch D, Karaman MM, Zhang J, Sui Y, Goldman JG, et al. High-spatial-resolution diffusion MRI in Parkinson disease: lateral asymmetry of the substantia Nigra. Radiology. 2019;291:149–57.
pubmed: 30777809
Goodman R. The Strengths and Difficulties Questionnaire: a research note. J Child Psychol Psychiatry. 1997;38:581–6.
pubmed: 9255702
Giraud R, Ta VT, Papadakis N, Manjon JV, Collins DL, Coupe P, et al. An Optimized PatchMatch for multi-scale and multi-feature label fusion. Neuroimage. 2016;124:770–82.
pubmed: 26244277
Wang Y, Xu Q, Li S, Li G, Zuo C, Liao S, et al. Gender differences in anomalous subcortical morphology for children with ADHD. Neurosci Lett. 2018;665:176–81.
pubmed: 29217259
Pinheiro JC, Bates DJ, Debroy SD, Sakar D. NLME: Linear and Nonlinear Mixed Effects Models. R package version. 2009;3:1–117.
Vijayakumar N, Mills KL, Alexander-Bloch A, Tamnes CK, Whittle S. Structural brain development: A review of methodological approaches and best practices. Dev Cogn Neurosci. 2018;33:129–48.
pubmed: 29221915
Raznahan A, Shaw PW, Lerch JP, Clasen LS, Greenstein D, Berman R, et al. Longitudinal four-dimensional mapping of subcortical anatomy in human development. Proc Natl Acad Sci USA. 2014;111:1592–7.
pubmed: 24474784
pmcid: 3910572
Paulsen DJ, Hallquist MN, Geier CF, Luna B. Effects of incentives, age, and behavior on brain activation during inhibitory control: a longitudinal fMRI study. Dev Cogn Neurosci. 2015;11:105–15.
pubmed: 25284272
Casey BJ. Beyond simple models of self-control to circuit-based accounts of adolescent behavior. Annu Rev Psychol. 2015;66:295–319.
pubmed: 25089362
Perneger TV. What’s wrong with Bonferroni adjustments. BMJ. 1998;316:1236–8.
pubmed: 9553006
pmcid: 1112991
Sankoh AJ, Huque MF, Dubey SD. Some comments on frequently used multiple endpoint adjustment methods in clinical trials. Stat Med. 1997;16:2529–42.
pubmed: 9403954
Hidding U, Gulberti A, Horn A, Buhmann C, Hamel W, Koeppen JA, et al. Impact of combined subthalamic nucleus and substantia nigra stimulation on neuropsychiatric symptoms in Parkinson’s disease patients. Parkinson’s Dis. 2017;2017:7306192.
Massey LA, Yousry TA. Anatomy of the substantia nigra and subthalamic nucleus on MR imaging. Neuroimaging Clin North Am. 2010;20:7–27.
Nambu A, Tokuno H, Takada M. Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci Res. 2002;43:111–7.
pubmed: 12067746
Mills KL, Goddings AL, Herting MM, Meuwese R, Blakemore SJ, Crone EA, et al. Structural brain development between childhood and adulthood: Convergence across four longitudinal samples. Neuroimage. 2016;141:273–81.
pubmed: 27453157
Dhamala E, Ooi LQR, Chen J, Kong R, Anderson KM, Chin R, et al. Proportional intracranial volume correction differentially biases behavioral predictions across neuroanatomical features, sexes, and development. Neuroimage. 2022;260:119485.
pubmed: 35843514
Bramen JE, Hranilovich JA, Dahl RE, Forbes EE, Chen J, Toga AW, et al. Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cereb Cortex. 2011;21:636–46.
pubmed: 20713504
Cole WR, Mostofsky SH, Larson JC, Denckla MB, Mahone EM. Age-related changes in motor subtle signs among girls and boys with ADHD. Neurology. 2008;71:1514–20.
pubmed: 18981373
pmcid: 2597066
Becker JB. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol, Biochem, Behav. 1999;64:803–12.
pubmed: 10593204
Wierenga L, Langen M, Ambrosino S, van Dijk S, Oranje B, Durston S. Typical development of basal ganglia, hippocampus, amygdala and cerebellum from age 7 to 24. Neuroimage. 2014;96:67–72.
pubmed: 24705201
Marcel R, David W, Martin S, Andreas W, Manfred G, Joseph C. et al. Structural alteration of substantia nigra in ADHD. Eur Child Adolesc Psychiatry. 2010;19:pS38
Durston S, Hulshoff Pol HE, Schnack HG, Buitelaar JK, Steenhuis MP, Minderaa RB, et al. Magnetic resonance imaging of boys with attention-deficit/hyperactivity disorder and their unaffected siblings. J Am Acad Child Adolesc Psychiatry. 2004;43:332–40.
pubmed: 15076267
Castellanos FX. A biased perspective on brain imaging of ADHD. Am J psychiatry. 2021;178:694–700.
pubmed: 34383564
Sterzer P, Stadler C. Neuroimaging of aggressive and violent behaviour in children and adolescents. Front Behav Neurosci. 2009;3:35.
pubmed: 19862349
pmcid: 2766784
Holz NE, Boecker-Schlier R, Buchmann AF, Blomeyer D, Jennen-Steinmetz C, Baumeister S, et al. Ventral striatum and amygdala activity as convergence sites for early adversity and conduct disorder. Soc Cogn Affect Neurosci. 2017;12:261–72.
pubmed: 27694318
Wallace GL, White SF, Robustelli B, Sinclair S, Hwang S, Martin A, et al. Cortical and subcortical abnormalities in youths with conduct disorder and elevated callous-unemotional traits. J Am Acad Child Adolesc Psychiatry. 2014;53:456–65.e451.
pubmed: 24655655
Scherfler C, Seppi K, Mair KJ, Donnemiller E, Virgolini I, Wenning GK, et al. Left hemispheric predominance of nigrostriatal dysfunction in Parkinson’s disease. Brain. 2012;135:3348–54.
pubmed: 23043142
Giedd JN, Clasen LS, Lenroot R, Greenstein D, Wallace GL, Ordaz S, et al. Puberty-related influences on brain development. Mol Cell Endocrinol. 2006;254–255:154–62.
pubmed: 16765510
Goddings AL, Mills KL, Clasen LS, Giedd JN, Viner RM, Blakemore SJ. The influence of puberty on subcortical brain development. Neuroimage. 2014;88:242–51.
pubmed: 24121203
Hu S, Pruessner JC, Coupe P, Collins DL. Volumetric analysis of medial temporal lobe structures in brain development from childhood to adolescence. Neuroimage. 2013;74:276–87.
pubmed: 23485848