Effects of age and sex on developmental neural networks of visual–spatial attention allocation

Compared to our understanding of the functional maturation of brain networks underlying complex cognitive abilities, hardly anything is known of the neurofunctional development of simpler cognitive abilities such as visuo-spatial attention allocation. Furthermore, nothing is known on the effect of gender on the functional development of attention allocation. This study employed event related functional magnetic resonance imaging to investigate effects of age, sex, and sex by age interactions on the brain activation of 63 males and females, between 13 to 38years, during a visual-spatial oddball task. Behaviourally, with increasing age, speed was traded for accuracy, indicative of a less impulsive performance style in older subjects. Increasing age was associated with progressively increased activation in typical areas of selective attention of lateral fronto-striatal and temporo-parietal brain regions. Sex difference analysis showed enhanced activation in right-hemispheric inferior frontal and superior temporal regions in females, and in left-hemispheric inferior temporo-parietal regions in males. Importantly, the age by sex interaction findings showed that these sex-dimorphic patterns of brain activation may be the result of underlying sex differences in the functional maturation of these brain regions, as females had sex-specific progressive age-correlations in the same right inferior fronto-striato-temporal areas, while male-specific age-correlations were in left medial temporal and parietal areas. The findings demonstrate progressive functional maturation of fronto-striato-parieto-temporal networks of the relatively simple function of attention allocation between early adolescence and mid-adulthood. They furthermore show that sex-dimorphic patterns of enhanced reliance on right inferior frontal, striatal and superior temporal regions in females and of left temporo-parietal regions in males during attention allocation may be the result of underlying sex differences in the functional maturation of these brain regions.

[1]  C. Pantelis,et al.  Normative Data From the Cantab. I: Development of Executive Function Over the Lifespan , 2003, Journal of clinical and experimental neuropsychology.

[2]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[3]  Rozmin Halari,et al.  Shared and disorder-specific prefrontal abnormalities in boys with pure attention-deficit/hyperactivity disorder compared to boys with pure CD during interference inhibition and attention allocation. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

[4]  Mark A Elliott,et al.  Hemodynamic responses in neural circuitries for detection of visual target and novelty: An event‐related fMRI study , 2007, Human brain mapping.

[5]  Jin Fan,et al.  Development of attentional networks: An fMRI study with children and adults , 2005, NeuroImage.

[6]  James M Provenzale,et al.  Age-related changes in neural activity during visual target detection measured by fMRI. , 2004, Cerebral cortex.

[7]  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.

[8]  R. Goebel,et al.  The functional neuroanatomy of target detection: an fMRI study of visual and auditory oddball tasks. , 1999, Cerebral cortex.

[9]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[10]  G. Pagnoni,et al.  Human Striatal Response to Salient Nonrewarding Stimuli , 2003, The Journal of Neuroscience.

[11]  K. R. Ridderinkhof,et al.  Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning , 2004, Brain and Cognition.

[12]  A. Toga,et al.  Mapping Changes in the Human Cortex throughout the Span of Life , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[13]  Michal Mikl,et al.  Combined event-related fMRI and intracerebral ERP study of an auditory oddball task , 2005, NeuroImage.

[14]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[15]  Chiara Nosarti,et al.  The neural basis of response inhibition and attention allocation as mediated by gestational age , 2009, Human brain mapping.

[16]  Shu-Chen Li,et al.  Electrophysiological correlates of selective attention: A lifespan comparison , 2008, BMC Neuroscience.

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

[18]  J T Enns,et al.  The development of selective attention: a life-span overview. , 1994, Acta psychologica.

[19]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[20]  T. Jernigan,et al.  Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study , 2002, Developmental medicine and child neurology.

[21]  J. M. Dabbs,et al.  Spatial Ability, Navigation Strategy, and Geographic Knowledge Among Men and Women , 1998 .

[22]  H. Karnath New insights into the functions of the superior temporal cortex , 2001, Nature Reviews Neuroscience.

[23]  Dinggang Shen,et al.  Puberty-related influences on brain development , 2006, Molecular and Cellular Endocrinology.

[24]  S. Petersen,et al.  Developmental changes in human cerebral functional organization for word generation. , 2005, Cerebral cortex.

[25]  V. Anderson,et al.  Assessing Executive Functions in Children: Biological, Psychological, and Developmental Considerations , 1998 .

[26]  Michael Petrides,et al.  Increased blood flow in the basal ganglia when using cues to direct attention , 1999, Experimental Brain Research.

[27]  C. Liston,et al.  Frontostriatal microstructure modulates efficient recruitment of cognitive control. , 2006, Cerebral cortex.

[28]  D. Amso,et al.  Development of cognitive control and executive functions from 4 to 13 years: Evidence from manipulations of memory, inhibition, and task switching , 2006, Neuropsychologia.

[29]  A. Nobre,et al.  Cognitive control of attention in the human brain: Insights from orienting attention to mental representations , 2006, Brain Research.

[30]  M. Brass,et al.  Involvement of the inferior frontal junction in cognitive control: Meta‐analyses of switching and Stroop studies , 2005, Human brain mapping.

[31]  James T. Enns,et al.  Attention, Development, and Psychopathology , 1997 .

[32]  Katya Rubia,et al.  Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection , 2003, NeuroImage.

[33]  Alan H. Wilman,et al.  Males and females differ in brain activation during cognitive tasks , 2006, NeuroImage.

[34]  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.

[35]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Korkman,et al.  Differential Development of Attention and Executive Functions in 3- to 12-Year-Old Finnish Children , 2001, Developmental neuropsychology.

[37]  Hans Forssberg,et al.  Increased Brain Activity in Frontal and Parietal Cortex Underlies the Development of Visuospatial Working Memory Capacity during Childhood , 2002, Journal of Cognitive Neuroscience.

[38]  Yihong Yang,et al.  A neural basis for the development of inhibitory control , 2002 .

[39]  Kevin Murphy,et al.  Individual differences in the functional neuroanatomy of inhibitory control , 2006, Brain Research.

[40]  D. Collins,et al.  A large sex difference on a two-dimensional mental rotation task. , 1997, Behavioral neuroscience.

[41]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[42]  Michal Mikl,et al.  Effective connectivity in target stimulus processing: A dynamic causal modeling study of visual oddball task , 2007, NeuroImage.

[43]  J. Gabrieli,et al.  Immature Frontal Lobe Contributions to Cognitive Control in Children Evidence from fMRI , 2002, Neuron.

[44]  S C Williams,et al.  Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. , 1997, Magnetic resonance imaging.

[45]  Michael J. Brammer,et al.  Temporal Lobe Dysfunction in Medication-Naïve Boys With Attention-Deficit/Hyperactivity Disorder During Attention Allocation and Its Relation to Response Variability , 2007, Biological Psychiatry.

[46]  J. Gore,et al.  Neural Correlates of the Attentional Blink , 2000, Neuron.

[47]  Daniel W. Hommer,et al.  Saccadic eye movements in normal children from 8 to 15 years of age: A developmental study of visuospatial attention , 1994, Journal of autism and developmental disorders.

[48]  Canan Karatekin,et al.  Development of attentional allocation in the dual task paradigm. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[49]  T A Carpenter,et al.  Colored noise and computational inference in neurophysiological (fMRI) time series analysis: Resampling methods in time and wavelet domains , 2001, Human brain mapping.

[50]  R. Benson,et al.  Responses to rare visual target and distractor stimuli using event-related fMRI. , 2000, Journal of neurophysiology.

[51]  S. Yantis,et al.  Cortical mechanisms of space-based and object-based attentional control , 2003, Current Opinion in Neurobiology.

[52]  John Duncan,et al.  Attentional functions of parietal and frontal cortex. , 2005, Cerebral cortex.

[53]  S. Yantis,et al.  Selective visual attention and perceptual coherence , 2006, Trends in Cognitive Sciences.

[54]  K. Kiehl,et al.  An event-related fMRI study of visual and auditory oddball tasks , 2001 .

[55]  C. Frith,et al.  Differential Activation of Right Superior Parietal Cortex and Intraparietal Sulcus by Spatial and Nonspatial Attention , 1998, NeuroImage.

[56]  Godfrey Pearlson,et al.  An adaptive reflexive processing model of neurocognitive function: supporting evidence from a large scale (n = 100) fMRI study of an auditory oddball task , 2005, NeuroImage.

[57]  M. Brammer,et al.  Linear age‐correlated functional development of right inferior fronto‐striato‐cerebellar networks during response inhibition and anterior cingulate during error‐related processes , 2007, Human brain mapping.

[58]  J. Downar,et al.  A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. , 2002, Journal of neurophysiology.

[59]  R. Sutherland,et al.  A characterization of performance by men and women in a virtual Morris water task: A large and reliable sex difference , 1998, Behavioural Brain Research.

[60]  E. Crone,et al.  Brain Regions Mediating Flexible Rule Use during Development , 2006, The Journal of Neuroscience.

[61]  D. Gitelman,et al.  The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts. , 2008, Cerebral cortex.

[62]  A. Nobre,et al.  Heterogeneity of Cingulate Contributions to Spatial Attention , 2001, NeuroImage.

[63]  B. Turetsky,et al.  An fMRI Study of Sex Differences in Regional Activation to a Verbal and a Spatial Task , 2000, Brain and Language.

[64]  Hongtu Zhu,et al.  A developmental fMRI study of self‐regulatory control , 2006, Human brain mapping.

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

[66]  J. Fletcher,et al.  Developmental changes in performance on tests of purported frontal lobe functioning , 1991 .

[67]  J. Stauder,et al.  The development of passive auditory novelty processing. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[68]  Michael J. Brammer,et al.  Developmental effects of reward on sustained attention networks , 2011, NeuroImage.

[69]  Vince D Calhoun,et al.  fMRI in an oddball task: effects of target-to-target interval. , 2005, Psychophysiology.

[70]  J. Wagemans,et al.  The Representation of Shape in the Context of Visual Object Categorization Tasks , 2000, NeuroImage.

[71]  Katherine A Loveland,et al.  Sex-related ERP differences in deviance detection. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[72]  Caroline F. Zink,et al.  Human striatal activation reflects degree of stimulus saliency , 2006, NeuroImage.

[73]  Margarete Delazer,et al.  Sex differences in cognitive functions , 2003 .

[74]  M. Keshavan,et al.  Sex differences in brain maturation during childhood and adolescence. , 2001, Cerebral cortex.

[75]  E. Bullmore,et al.  Methods for diagnosis and treatment of stimulus‐correlated motion in generic brain activation studies using fMRI , 1999, Human brain mapping.

[76]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

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

[78]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.

[79]  Leanne M Williams,et al.  Neural synchrony and gray matter variation in human males and females: integration of 40 Hz gamma synchrony and MRI measures. , 2005, Journal of integrative neuroscience.

[80]  Antao Chen,et al.  Gender differences in behavioral inhibitory control: ERP evidence from a two-choice oddball task. , 2008, Psychophysiology.

[81]  James R. Booth,et al.  Neural development of selective attention and response inhibition , 2003, NeuroImage.

[82]  Gary H. Glover,et al.  A Developmental fMRI Study of the Stroop Color-Word Task , 2002, NeuroImage.

[83]  M. Brammer,et al.  Progressive increase of frontostriatal brain activation from childhood to adulthood during event‐related tasks of cognitive control , 2006, Human brain mapping.

[84]  G. Pearlson,et al.  Sex differences in the inferior parietal lobule. , 1999, Cerebral cortex.

[85]  D. V. Cramon,et al.  Subprocesses of Performance Monitoring: A Dissociation of Error Processing and Response Competition Revealed by Event-Related fMRI and ERPs , 2001, NeuroImage.

[86]  R. Woods,et al.  Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. , 2007, Cerebral cortex.

[87]  K. Schaie The course of adult intellectual development. , 1994, The American psychologist.

[88]  V. Menon,et al.  Neural basis of protracted developmental changes in visuo-spatial working memory , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[89]  J. Pratt,et al.  Playing an Action Video Game Reduces Gender Differences in Spatial Cognition , 2007, Psychological science.

[90]  P. Goldman-Rakic,et al.  Prefrontal Activation Evoked by Infrequent Target and Novel Stimuli in a Visual Target Detection Task: An Event-Related Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[91]  Suzanne E. Welcome,et al.  Mapping cortical change across the human life span , 2003, Nature Neuroscience.

[92]  Adam M. Brickman,et al.  Volume of the cingulate and outcome in schizophrenia , 2005, Schizophrenia Research.

[93]  Mijna Hadders-Algra,et al.  Ontogeny of the human central nervous system: what is happening when? , 2006, Early human development.

[94]  Laurie E. Cutting,et al.  Developmental sex differences in basic visuospatial processing: Differences in strategy use? , 2009, Neuroscience Letters.

[95]  T. Klingberg,et al.  Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. , 2003, Brain research. Cognitive brain research.

[96]  B. Turetsky,et al.  Reduced gray matter volume in schizophrenia. , 1999, Archives of general psychiatry.

[97]  Vicki A. Anderson,et al.  Development of Executive Functions Through Late Childhood and Adolescence in an Australian Sample , 2001, Developmental neuropsychology.

[98]  Jonathan D. Cohen,et al.  A Developmental Functional MRI Study of Prefrontal Activation during Performance of a Go-No-Go Task , 1997, Journal of Cognitive Neuroscience.

[99]  Irwin Feinberg,et al.  Sleep EEG evidence of sex differences in adolescent brain maturation. , 2005, Sleep.

[100]  E. Bullmore,et al.  Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI , 2000, Neuroscience & Biobehavioral Reviews.

[101]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[103]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[104]  B. Ardekani,et al.  Functional magnetic resonance imaging of brain activity in the visual oddball task. , 2002, Brain research. Cognitive brain research.

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