Thalamocortical functional connectivity in youth with attention-deficit/hyperactivity disorder

Background: Few studies have empirically tested the relationships between anatomically defined thalamic nuclei and functionally defined cortical networks, and little is known about their implications in attention-deficit/hyperactivity disorder (ADHD). This study aimed to investigate the functional connectivity of the thalamus in youth with ADHD, using both anatomically and functionally defined thalamic seed regions. Methods: Resting-state functional MRIs obtained from the publicly available ADHD-200 database were analyzed. Thalamic seed regions were defined functionally and anatomically based on Yeo’s 7 resting-state-network parcellation atlas and the AAL3 atlas, respectively. Functional connectivity maps of the thalamus were extracted, and thalamocortical functional connectivity was compared between youth with and without ADHD. Results: Using the functionally defined seeds, significant group differences in thalamocortical functional connectivity and significant negative correlations between thalamocortical connectivity and ADHD symptom severity were observed within the boundaries of corresponding large-scale networks. However, in the analysis using the anatomically defined thalamic seeds, significant group differences in connectivity and significant positive correlations were observed outside the expected boundaries of major anatomic projections. The thalamocortical connectivity originating from the lateral geniculate nuclei of the thalamus was significantly correlated with age in youth with ADHD. Limitations: The small sample size and smaller proportion of girls were limiting factors. Conclusion: Thalamocortical functional connectivity based on the intrinsic network architecture of the brain appears to be clinically relevant in ADHD. The positive association between thalamocortical functional connectivity and ADHD symptom severity may represent a compensatory process recruiting an alternative neural network.

[1]  Elizabeth B. Owens,et al.  Variable Patterns of Remission From ADHD in the Multimodal Treatment Study of ADHD. , 2021, The American journal of psychiatry.

[2]  P. Shaw,et al.  Adolescent Attention-Deficit/Hyperactivity Disorder: Understanding Teenage Symptom Trajectories , 2020, Biological Psychiatry.

[3]  Jianfeng Feng,et al.  Automated anatomical labelling atlas 3 , 2020, NeuroImage.

[4]  B T Thomas Yeo,et al.  Towards a Universal Taxonomy of Macro-scale Functional Human Brain Networks , 2019, Brain Topography.

[5]  André J. W. van der Kouwe,et al.  A probabilistic atlas of the human thalamic nuclei combining ex vivo MRI and histology , 2018, NeuroImage.

[6]  N. Wenderoth,et al.  Structural Basis of Large-Scale Functional Connectivity in the Mouse , 2017, The Journal of Neuroscience.

[7]  Heath R. Pardoe,et al.  Motion and morphometry in clinical and nonclinical populations , 2016, NeuroImage.

[8]  Yufeng Zang,et al.  DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging , 2016, Neuroinformatics.

[9]  Daniel S. Margulies,et al.  The Neuro Bureau ADHD-200 Preprocessed repository , 2016, NeuroImage.

[10]  Maarten Mennes,et al.  The executive control network and symptomatic improvement in attention-deficit/hyperactivity disorder , 2015, Cortex.

[11]  M. Sigman,et al.  Signature of consciousness in the dynamics of resting-state brain activity , 2015, Proceedings of the National Academy of Sciences.

[12]  C. Sripada,et al.  Lag in maturation of the brain’s intrinsic functional architecture in attention-deficit/hyperactivity disorder , 2014, Proceedings of the National Academy of Sciences.

[13]  J. Posner,et al.  Connecting the Dots: A Review of Resting Connectivity MRI Studies in Attention-Deficit/Hyperactivity Disorder , 2014, Neuropsychology Review.

[14]  Y. Stern,et al.  Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve , 2013, Trends in Cognitive Sciences.

[15]  Cheuk Y. Tang,et al.  Thalamo-cortical activation and connectivity during response preparation in adults with persistent and remitted ADHD. , 2013, The American journal of psychiatry.

[16]  Hae-Jeong Park,et al.  Functional connectivity‐based identification of subdivisions of the basal ganglia and thalamus using multilevel independent component analysis of resting state fMRI , 2013, Human brain mapping.

[17]  M. Walter,et al.  Functional mapping of thalamic nuclei and their integration into cortico-striatal-thalamo-cortical loops via ultra-high resolution imaging—from animal anatomy to in vivo imaging in humans , 2013, Front. Neurosci..

[18]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[19]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[20]  F. Xavier Castellanos,et al.  Large-scale brain systems in ADHD: beyond the prefrontal–striatal model , 2012, Trends in Cognitive Sciences.

[21]  Kathryn L. Mills,et al.  Altered Cortico-Striatal–Thalamic Connectivity in Relation to Spatial Working Memory Capacity in Children with ADHD , 2012, Front. Psychiatry.

[22]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[23]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[24]  Sebastian Seifert,et al.  Thalamocingulate Interactions In Performance Monitoring , 2011, The Journal of Neuroscience.

[25]  Timothy Edward John Behrens,et al.  Topography of connections between human prefrontal cortex and mediodorsal thalamus studied with diffusion tractography , 2010, NeuroImage.

[26]  Kerstin Konrad,et al.  Is the ADHD brain wired differently? A review on structural and functional connectivity in attention deficit hyperactivity disorder , 2010, Human brain mapping.

[27]  Stewart H. Mostofsky,et al.  Increased intra-individual reaction time variability in attention-deficit/hyperactivity disorder across response inhibition tasks with different cognitive demands , 2009, Neuropsychologia.

[28]  M. Fox,et al.  Intrinsic functional relations between human cerebral cortex and thalamus. , 2008, Journal of neurophysiology.

[29]  B. Horta,et al.  The worldwide prevalence of ADHD: a systematic review and metaregression analysis. , 2007, The American journal of psychiatry.

[30]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[31]  Bruce D. McCandliss,et al.  Response Anticipation and Response Conflict: An Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2007, The Journal of Neuroscience.

[32]  J. Schweitzer,et al.  Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature. , 2006, Clinical psychology review.

[33]  Joseph Biederman,et al.  The age-dependent decline of attention deficit hyperactivity disorder: a meta-analysis of follow-up studies , 2005, Psychological Medicine.

[34]  Naomi Hasegawa,et al.  Thalamocortical and intracortical connections of monkey cingulate motor areas , 2003, The Journal of comparative neurology.

[35]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[36]  Y. Stern What is cognitive reserve? Theory and research application of the reserve concept , 2002, Journal of the International Neuropsychological Society.

[37]  David P. Friedman,et al.  Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the macaque , 1986, The Journal of comparative neurology.

[38]  P. Goldman-Rakic,et al.  The primate mediodorsal (MD) nucleus and its projection to the frontal lobe , 1985, The Journal of comparative neurology.

[39]  F Mauguiere,et al.  The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis. , 1980, Brain : a journal of neurology.

[40]  E. G. Jones,et al.  Differential thalamic relationships of sensory‐motor and parietal cortical fields in monkeys , 1979, The Journal of comparative neurology.

[41]  Duke Tanaka,et al.  Thalamic projections of the dorsomedial prefrontal cortex in the rhesus monkey (Macaca mulatta) , 1976, Brain Research.

[42]  T. J. Tobias,et al.  Afferents to prefrontal cortex from the thalamic mediodorsal nucleus in the rhesus monkey , 1975, Brain Research.

[43]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. , 1969, Brain : a journal of neurology.

[44]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[45]  R. Buckner,et al.  The organization of the human striatum estimated by intrinsic functional connectivity. , 2012, Journal of neurophysiology.

[46]  Christopher L. Asplund,et al.  The organization of the human cerebellum estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[47]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[48]  Yaakov Stern,et al.  Cognitive Reserve: Implications for Assessment and Intervention , 2013, Folia Phoniatrica et Logopaedica.

[49]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[50]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. 3. Thalamic connexions. , 1970, Brain : a journal of neurology.