Resting States Are Resting Traits – An fMRI Study of Sex Differences and Menstrual Cycle Effects in Resting State Cognitive Control Networks

To what degree resting state fMRI is stable or susceptible to internal mind states of the individual is currently an issue of debate. To address this issue, the present study focuses on sex differences and investigates whether resting state fMRI is stable in men and women or changes within relative short-term periods (i.e., across the menstrual cycle). Due to the fact that we recently reported menstrual cycle effects on cognitive control based on data collected during the same sessions, the current study is particularly interested in fronto-parietal resting state networks. Resting state fMRI was measured in sixteen women during three different cycle phases (menstrual, follicular, and luteal). Fifteen men underwent three sessions in corresponding time intervals. We used independent component analysis to identify four fronto-parietal networks. The results showed sex differences in two of these networks with women exhibiting higher functional connectivity in general, including the prefrontal cortex. Menstrual cycle effects on resting states were non-existent. It is concluded that sex differences in resting state fMRI might reflect sexual dimorphisms in the brain rather than transitory activating effects of sex hormones on the functional connectivity in the resting brain.

[1]  Benjamin J. Shannon,et al.  Coherent spontaneous activity identifies a hippocampal-parietal memory network. , 2006, Journal of neurophysiology.

[2]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[3]  Kenneth Hugdahl,et al.  Language lateralization and cognitive control across the menstrual cycle assessed with a dichotic-listening paradigm , 2012, Psychoneuroendocrinology.

[4]  O. Güntürkün,et al.  Steroid fluctuations modify functional cerebral asymmetries: the hypothesis of progesterone-mediated interhemispheric decoupling , 2000, Neuropsychologia.

[5]  A. Malhotra,et al.  Sex differences in frontal lobe white matter microstructure: a DTI study , 2003, Neuroreport.

[6]  L. Nyberg,et al.  Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration? , 2005, Consciousness and Cognition.

[7]  L. Katz,et al.  Sex differences in the functional organization of the brain for language , 1995, Nature.

[8]  W. Sturm,et al.  Menstrual cycle effects on selective attention and its underlying cortical networks , 2014, Neuroscience.

[9]  René Westerhausen,et al.  Reactive cognitive-control processes in free-report consonant–vowel dichotic listening , 2013, Brain and Cognition.

[10]  Kenneth Hugdahl,et al.  A critical re-examination of sexual dimorphism in the corpus callosum microstructure , 2011, NeuroImage.

[11]  In Chan Song,et al.  Tractography-guided statistics (TGIS) in diffusion tensor imaging for the detection of gender difference of fiber integrity in the midsagittal and parasagittal corpora callosa , 2007, NeuroImage.

[12]  M. McCarthy,et al.  Mechanisms Mediating Oestradiol Modulation of the Developing Brain , 2008, Journal of neuroendocrinology.

[13]  M. Corbetta,et al.  Episodic Memory Retrieval, Parietal Cortex, and the Default Mode Network: Functional and Topographic Analyses , 2011, The Journal of Neuroscience.

[14]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[15]  Daniel Voyer,et al.  Sex differences in mental rotation: Top–down versus bottom–up processing , 2006, NeuroImage.

[16]  P. Fransson How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations , 2006, Neuropsychologia.

[17]  K. Davis,et al.  Cognitive and default‐mode resting state networks: Do male and female brains “rest” differently? , 2010, Human brain mapping.

[18]  G. D. de Courten-Myers The human cerebral cortex: gender differences in structure and function. , 1999, Journal of neuropathology and experimental neurology.

[19]  Kenneth Hugdahl,et al.  An fMRI study of phonological and spatial working memory using identical stimuli. , 2008, Scandinavian journal of psychology.

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

[21]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[22]  M. Hausmann Hemispheric asymmetry in spatial attention across the menstrual cycle , 2005, Neuropsychologia.

[23]  Alan C. Evans,et al.  Growing Together and Growing Apart: Regional and Sex Differences in the Lifespan Developmental Trajectories of Functional Homotopy , 2010, The Journal of Neuroscience.

[24]  A. Lundervold,et al.  Functional magnetic resonance imaging (fMRI) study of sex differences in a mental rotation task. , 2000, Medical science monitor : international medical journal of experimental and clinical research.

[25]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[26]  D. Lewis,et al.  Quantitative methods in psychology , 1950 .

[27]  O. Güntürkün,et al.  Sex differences in oral asymmetries during wordrepetition , 1998, Neuropsychologia.

[28]  I. J. Kirk,et al.  Sex hormonal modulation of interhemispheric transfer time , 2013, Neuropsychologia.

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

[30]  Mick Brammer,et al.  Sex-dependent age modulation of frontostriatal and temporo-parietal activation during cognitive control , 2009, NeuroImage.

[31]  E M Reiman,et al.  The application of positron emission tomography to the study of the normal menstrual cycle. , 1996, Human reproduction.

[32]  Jen-Chuen Hsieh,et al.  The resting frontal alpha asymmetry across the menstrual cycle: A magnetoencephalographic study , 2008, Hormones and Behavior.

[33]  Jorge Sepulcre,et al.  Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors , 2009, Proceedings of the National Academy of Sciences.

[34]  C. Sisk,et al.  Pubertal hormones organize the adolescent brain and behavior , 2005, Frontiers in Neuroendocrinology.

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

[36]  Simon B. Eickhoff,et al.  One-year test–retest reliability of intrinsic connectivity network fMRI in older adults , 2012, NeuroImage.

[37]  G. McKitterick,et al.  THE MAGNITUDE OF π , 1983 .

[38]  Nikos Makris,et al.  Sex differences in prefrontal cortical brain activity during fMRI of auditory verbal working memory. , 2005, Neuropsychology.

[39]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[40]  K. Hugdahl,et al.  Sex differences in visuo-spatial processing: An fMRI study of mental rotation , 2006, Neuropsychologia.

[41]  W. Sturm,et al.  Dynamic changes in functional cerebral connectivity of spatial cognition during the menstrual cycle , 2011, Human brain mapping.

[42]  Esther Gómez-Gil,et al.  Effects of androgenization on the white matter microstructure of female-to-male transsexuals. A diffusion tensor imaging study , 2012, Psychoneuroendocrinology.

[43]  N. Geschwind,et al.  Cerebral lateralization. Biological mechanisms, associations, and pathology: III. A hypothesis and a program for research. , 1985, Archives of neurology.

[44]  André Aleman,et al.  Do women really have more bilateral language representation than men? A meta-analysis of functional imaging studies. , 2004, Brain : a journal of neurology.

[45]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[46]  C. Gross,et al.  Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. , 1998, Journal of neurophysiology.

[47]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[48]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[49]  N Jon Shah,et al.  Assessment of reliability in functional imaging studies , 2003, Journal of magnetic resonance imaging : JMRI.

[50]  Massimo Filippi,et al.  The organization of intrinsic brain activity differs between genders: A resting‐state fMRI study in a large cohort of young healthy subjects , 2013, Human brain mapping.

[51]  M. Hiscock,et al.  Is there a sex difference in human laterality? III. An exhaustive survey of tactile laterality studies from six neuropsychology journals. , 1994 .

[52]  Yong He,et al.  Hemisphere- and gender-related differences in small-world brain networks: A resting-state functional MRI study , 2011, NeuroImage.

[53]  M. D’Esposito,et al.  Estrogen Shapes Dopamine-Dependent Cognitive Processes: Implications for Women's Health , 2011, The Journal of Neuroscience.

[54]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[55]  Jessica A. Turner,et al.  Reliability of the amplitude of low-frequency fluctuations in resting state fMRI in chronic schizophrenia , 2012, Psychiatry Research: Neuroimaging.

[56]  N. Volkow,et al.  Laterality patterns of brain functional connectivity: gender effects. , 2012, Cerebral cortex.

[57]  B. Pakkenberg,et al.  Neocortical neuron number in humans: Effect of sex and age , 1997, The Journal of comparative neurology.

[58]  G. Jackson,et al.  Effect of prior cognitive state on resting state networks measured with functional connectivity , 2005, Human brain mapping.

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

[60]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[61]  E. Baracat,et al.  Effects of estradiol on the cognitive function of postmenopausal women. , 2008, Maturitas.

[62]  N. Geschwind,et al.  Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. , 1985, Archives of neurology.

[63]  Andreas Heinz,et al.  Test–retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures , 2012, NeuroImage.

[64]  Onur Güntürkün,et al.  Interhemispheric interaction during the menstrual cycle , 2008, Neuropsychologia.

[65]  Jane E. Joseph,et al.  Influence of estradiol on functional brain organization for working memory , 2012, NeuroImage.

[66]  B. Harrison,et al.  Modulation of Brain Resting-State Networks by Sad Mood Induction , 2008, PloS one.

[67]  Kenneth Hugdahl,et al.  Sex differences in language asymmetry are age-dependent and small: A large-scale, consonant–vowel dichotic listening study with behavioral and fMRI data , 2013, Cortex.

[68]  S. Golaszewski,et al.  Sex differences in brain activation pattern during a visuospatial cognitive task: a functional magnetic resonance imaging study in healthy volunteers , 2003, Neuroscience Letters.

[69]  R. Bluhm,et al.  Default mode network connectivity: effects of age, sex, and analytic approach , 2008, Neuroreport.

[70]  A. Kersting,et al.  Functional anatomy of visuo-spatial working memory during mental rotation is influenced by sex, menstrual cycle, and sex steroid hormones , 2007, Neuropsychologia.

[71]  S. Kaufman Sex differences in mental rotation and spatial visualization ability: Can they be accounted for by differences in working memory capacity? , 2007 .

[72]  Gabrielle M. de Courten-Myers,et al.  The human cerebral cortex: gender differences in structure and function. , 1999 .

[73]  François Bellavance,et al.  Proton Magnetic Resonance Spectroscopy Measurement of Brain Glutamate Levels in Premenstrual Dysphoric Disorder , 2008, Biological Psychiatry.

[74]  Jacob Cohen,et al.  QUANTITATIVE METHODS IN PSYCHOLOGY A Power Primer , 1992 .

[75]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[76]  Sukhwinder S. Shergill,et al.  Gender Differences in White Matter Microstructure , 2012, PloS one.

[77]  Oliver T. Wolf,et al.  Endogenous Estradiol and Testosterone Levels Are Associated with Cognitive Performance in Older Women and Men , 2002, Hormones and Behavior.

[78]  M. Casey,et al.  Girls who use “masculine” problem-solving strategies on a spatial task: Proposed genetic and environmental factors , 1991, Brain and Cognition.

[79]  W. C. Young,et al.  Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. , 1959, Endocrinology.

[80]  Biyu J. He,et al.  Loss of Resting Interhemispheric Functional Connectivity after Complete Section of the Corpus Callosum , 2008, The Journal of Neuroscience.

[81]  Rex E. Jung,et al.  A Baseline for the Multivariate Comparison of Resting-State Networks , 2011, Front. Syst. Neurosci..

[82]  G. Moore,et al.  Prefrontal cortex as the site of estrogen's effect on cognition , 2001, Psychoneuroendocrinology.

[83]  C. Dickey,et al.  Investigation of Long-Term Reproducibility of Intrinsic Connectivity Network Mapping: A Resting-State fMRI Study , 2012, American Journal of Neuroradiology.

[84]  Georg Northoff,et al.  How is our self related to midline regions and the default-mode network? , 2011, NeuroImage.

[85]  O. Güntürkün,et al.  Transcallosal inhibition across the menstrual cycle: A TMS study , 2006, Clinical Neurophysiology.

[86]  B. Biswal,et al.  The resting brain: unconstrained yet reliable. , 2009, Cerebral cortex.

[87]  Lisa A. Kilpatrick,et al.  Oral contraceptive pill use and menstrual cycle phase are associated with altered resting state functional connectivity , 2014, NeuroImage.

[88]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[89]  Maximilian Reiser,et al.  Classifying fMRI-derived resting-state connectivity patterns according to their daily rhythmicity , 2013, NeuroImage.

[90]  Jacob Cohen,et al.  A power primer. , 1992, Psychological bulletin.

[91]  Ting Li,et al.  Gender-specific hemodynamics in prefrontal cortex during a verbal working memory task by near-infrared spectroscopy , 2010, Behavioural Brain Research.

[92]  J. Jonides,et al.  Dissociating verbal and spatial working memory using PET. , 1996, Cerebral cortex.

[93]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[94]  Ursula Gather,et al.  Functional cerebral asymmetries during the menstrual cycle: a cross-sectional and longitudinal analysis , 2002, Neuropsychologia.

[95]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[96]  T. Kellermann,et al.  Estradiol Modulates Functional Brain Organization during the Menstrual Cycle: An Analysis of Interhemispheric Inhibition , 2008, The Journal of Neuroscience.

[97]  Geoff Sanders,et al.  Verbal and music dichotic listening tasks reveal variations in functional cerebral asymmetry across the menstrual cycle that are phase and task dependent , 1998, Neuropsychologia.

[98]  D. Voyer,et al.  On the magnitude of laterality effects and sex differences in functional lateralities. , 1996, Laterality.