Sex Differences in Fiber Connection between the Striatum and Subcortical and Cortical Regions

The striatum is an important subcortical structure with extensive connections to other regions of the brain. These connections are believed to play important roles in behaviors such as reward-related processes and impulse control, which show significant sex differences. However, little is known about sex differences in the striatum-projected fiber connectivity. The current study examined sex differences between 50 Chinese males and 79 Chinese females in their fiber connections between the striatum and nine selected cortical and subcortical regions. Despite overall similarities, males showed stronger fiber connections between the left caudate and rostral cingulate cortex, between the right putamen and the lateral orbitofrontal cortex, between the bilateral putamen and the ventro-lateral prefrontal cortex, and between the right caudate and the ventro-lateral prefrontal cortex, whereas females showed stronger fiber connections between the right putamen and the dorsolateral prefrontal cortex, between bilateral caudate and hippocampus, and between the left putamen and hippocampus. These findings help us to understand sex differences in the striatum-projected fiber connections and their implications for sex differences in behaviors.

[1]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[2]  若菜 勢津 Fiber tract-based atlas of human white matter anatomy , 2006 .

[3]  Wieslaw Lucjan Nowinski,et al.  Three-Dimensional Interactive and Stereotactic Human Brain Atlas of White Matter Tracts , 2011, Neuroinformatics.

[4]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[5]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[6]  Timothy Edward John Behrens,et al.  Connectivity-based functional analysis of dopamine release in the striatum using diffusion-weighted MRI and positron emission tomography. , 2014, Cerebral cortex.

[7]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[8]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[9]  L. Fattore,et al.  Reward processing and drug addiction: does sex matter? , 2015, Front. Neurosci..

[10]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[11]  Self-Concept Variables Sex Differences in , 2016 .

[12]  J. Jacobs,et al.  Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. , 2001, Cerebral cortex.

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

[14]  Matthew L. Dixon Cognitive control, emotional value, and the lateral prefrontal cortex , 2015, Front. Psychol..

[15]  T. Verstynen,et al.  Converging Structural and Functional Connectivity of Orbitofrontal, Dorsolateral Prefrontal, and Posterior Parietal Cortex in the Human Striatum , 2014, The Journal of Neuroscience.

[16]  Jung-Lung Hsu,et al.  Gender differences and age-related white matter changes of the human brain: A diffusion tensor imaging study , 2008, NeuroImage.

[17]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[18]  M. Mather,et al.  Gender differences in reward-related decision processing under stress. , 2012, Social cognitive and affective neuroscience.

[19]  Michael X. Cohen,et al.  Connectivity-based segregation of the human striatum predicts personality characteristics , 2009, Nature Neuroscience.

[20]  B. Turetsky,et al.  Sex Differences in Brain Gray and White Matter in Healthy Young Adults: Correlations with Cognitive Performance , 1999, The Journal of Neuroscience.

[21]  D. Halpern,et al.  The new science of cognitive sex differences , 2014, Trends in Cognitive Sciences.

[22]  Stephen M. Smith,et al.  Permutation inference for the general linear model , 2014, NeuroImage.

[23]  Wolfgang M. Pauli,et al.  Regional specialization within the human striatum for diverse psychological functions , 2016, Proceedings of the National Academy of Sciences.

[24]  Gina Rippon,et al.  Recommendations for sex/gender neuroimaging research: key principles and implications for research design, analysis, and interpretation , 2014, Front. Hum. Neurosci..

[25]  Naoto Hayashi,et al.  Sex dimorphism in the white matter: Fractional anisotropy and brain size , 2014, Journal of magnetic resonance imaging : JMRI.

[26]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[27]  P. Falkai,et al.  A functional neuroimaging study assessing gender differences in the neural mechanisms underlying the ability to resist impulsive desires , 2012, Brain Research.

[28]  Qi Wang,et al.  Gender and emotion in everyday event memory , 2013, Memory.

[29]  M. Roesch,et al.  From ventral-medial to dorsal-lateral striatum: Neural correlates of reward-guided decision-making , 2015, Neurobiology of Learning and Memory.

[30]  N. Makris,et al.  Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. , 2001, Cerebral cortex.

[31]  Timothy Edward John Behrens,et al.  Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI , 2007, The Journal of Neuroscience.

[32]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[33]  James N. Porter,et al.  Age-related changes in the intrinsic functional connectivity of the human ventral vs. dorsal striatum from childhood to middle age , 2014, Developmental Cognitive Neuroscience.

[34]  Daphna Joel,et al.  Male or Female? Brains are Intersex , 2011, Front. Integr. Neurosci..

[35]  Gina Rippon,et al.  Plasticity, plasticity, plasticity…and the rigid problem of sex , 2013, Trends in Cognitive Sciences.

[36]  Thomas R. Barrick,et al.  Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection , 2008, NeuroImage.

[37]  Nadia M. Brashier,et al.  Memory Meets Control in Hippocampal and Striatal Binding of Stimuli, Responses, and Attentional Control States , 2015, The Journal of Neuroscience.

[38]  G. Egan,et al.  Connectivity-based segmentation of the striatum in Huntington's disease: Vulnerability of motor pathways , 2011, Neurobiology of Disease.

[39]  Susumu Mori,et al.  Fiber tracking: principles and strategies – a technical review , 2002, NMR in biomedicine.

[40]  L. Cahill Why sex matters for neuroscience , 2006, Nature Reviews Neuroscience.

[41]  Alan C. Evans,et al.  Age- and Gender-Related Differences in the Cortical Anatomical Network , 2009, The Journal of Neuroscience.

[42]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[43]  S. Arver,et al.  Sex differences in the human brain and the impact of sex chromosomes and sex hormones. , 2013, Cerebral cortex.

[44]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[45]  G. Elston Pyramidal Cells of the Frontal Lobe: All the More Spinous to Think With , 2000, The Journal of Neuroscience.

[46]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[47]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[48]  N. Swindale,et al.  Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans , 2004, Annals of neurology.

[49]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[50]  K. Cosgrove,et al.  Evolving Knowledge of Sex Differences in Brain Structure, Function, and Chemistry , 2007, Biological Psychiatry.

[51]  Daniel C Alexander,et al.  Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[52]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[53]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[54]  Bonnie J Nagel,et al.  The impact of sex, puberty, and hormones on white matter microstructure in adolescents. , 2012, Cerebral cortex.

[55]  S. Leh,et al.  Fronto-striatal connections in the human brain: A probabilistic diffusion tractography study , 2007, Neuroscience Letters.

[56]  Janet Shibley Hyde,et al.  Gender similarities and differences. , 2014, Annual review of psychology.

[57]  Daniella J. Furman,et al.  Menstrual cycle phase modulates reward-related neural function in women , 2007, Proceedings of the National Academy of Sciences.

[58]  Jun Li,et al.  Fiber connectivity between the striatum and cortical and subcortical regions is associated with temperaments in Chinese males , 2014, NeuroImage.

[59]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[60]  Matthew L. Dixon,et al.  The lateral prefrontal cortex and complex value-based learning and decision making , 2014, Neuroscience & Biobehavioral Reviews.

[61]  P. Calabresi,et al.  Striatum–hippocampus balance: From physiological behavior to interneuronal pathology , 2011, Progress in Neurobiology.

[62]  N. Daw,et al.  Fronto-striatal organization: Defining functional and microstructural substrates of behavioural flexibility , 2016, Cortex.

[63]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[64]  Timothy Edward John Behrens,et al.  Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. , 2005, Cerebral cortex.