Individual differences in anterior cingulate/paracingulate morphology are related to executive functions in healthy males.

The neuropsychological correlates of inter-individual variations in cortical folding are poorly understood. Anterior cingulate (AC) cortex is one region characterized by considerable variability, particularly with respect to the paracingulate sulcus (PCS), which is present in only 30-60% of individuals and more commonly found in the left cerebral hemisphere. To investigate whether inter-individual differences in this PCS asymmetry are related to cognitive performance, we classified 30 healthy right-handed males as displaying either a leftward, rightward or symmetric pattern of folding based on the incidence and extent of the PCS in each hemisphere, and compared their performance on tasks engaging executive cognitive processes associated with frontal lobe function. We found that the more common leftward PCS asymmetry was associated with better performance across verbal and non-verbal executive tasks, but that PCS variability had no effect on tasks less dependent on executive functions. These results suggest that the leftward pattern of folding is associated with a non-specific performance advantage on cognitively demanding executive function tasks, possibly due to differences in functional interactions between AC/paracingulate cortex and connected frontal regions. It therefore appears that normal variations in brain morphology are associated with individual differences in cognitive abilities.

[1]  Lisa Koski,et al.  Erratum to: Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis , 2000, Experimental Brain Research.

[2]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

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

[4]  S. Berkovic,et al.  Lateralization of verbal memory and unilateral hippocampal sclerosis: evidence of task-specific effects. , 1993, Journal of clinical and experimental neuropsychology.

[5]  A W Toga,et al.  Sulcal variability in the Alzheimer's brain , 1998, Neurology.

[6]  J. Desmond,et al.  Prefrontal regions involved in keeping information in and out of mind. , 2001, Brain : a journal of neurology.

[7]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[8]  W. Welker Why Does Cerebral Cortex Fissure and Fold , 1990 .

[9]  A. Galaburda,et al.  Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. , 1993, Cerebral cortex.

[10]  E. Mulvey,et al.  Regression analyses of counts and rates: Poisson, overdispersed Poisson, and negative binomial models. , 1995, Psychological bulletin.

[11]  P. Diggle Analysis of Longitudinal Data , 1995 .

[12]  R. Passingham Attention to action. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[13]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  A. Schleicher,et al.  The ontogeny of human gyrification. , 1995, Cerebral cortex.

[15]  Alan C. Evans,et al.  Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. , 1996, Cerebral cortex.

[16]  T. Robbins,et al.  Planning and spatial working memory following frontal lobe lesions in man , 1990, Neuropsychologia.

[17]  A. Dagher,et al.  Mapping the network for planning: a correlational PET activation study with the Tower of London task. , 1999, Brain : a journal of neurology.

[18]  S. Zeger,et al.  Longitudinal data analysis using generalized linear models , 1986 .

[19]  Camilla Anne Czubaj The Wechsler Adult Intelligence Scale - Revised, Revisited , 1996 .

[20]  A. Thiel,et al.  Individual Functional Anatomy of Verb Generation , 1996, NeuroImage.

[21]  B. Milner,et al.  Interhemispheric differences in the localization of psychological processes in man. , 1971, British medical bulletin.

[22]  David C Reutens,et al.  Verbal memory in left temporal lobe epilepsy: Evidence for task‐related localization , 2002, Annals of neurology.

[23]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[24]  A. Toga,et al.  Three-Dimensional Statistical Analysis of Sulcal Variability in the Human Brain , 1996, The Journal of Neuroscience.

[25]  Bradley R Postle,et al.  The dependence of span and delayed-response performance on prefrontal cortex , 1999, Neuropsychologia.

[26]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[27]  小野 道夫,et al.  Atlas of the Cerebral Sulci , 1990 .

[28]  J. Scannell Determining cortical landscapes , 1997, Nature.

[29]  G. Jackson,et al.  A Neurocognitive Account of Frontal Lobe Involvement in Orthographic Lexical Retrieval: An fMRI Study , 2001, NeuroImage.

[30]  A. Schleicher,et al.  Motor cortex and hand motor skills: Structural compliance in the human brain , 1997, Human brain mapping.

[31]  F. Gilles,et al.  Gyral development of the human brain. , 1977, Annals of Neurology.

[32]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[33]  D. Stuss,et al.  The effects of focal anterior and posterior brain lesions on verbal fluency , 1998, Journal of the International Neuropsychological Society.

[34]  P. Maruff,et al.  Hemispheric and gender-related differences in the gross morphology of the anterior cingulate/paracingulate cortex in normal volunteers: an MRI morphometric study. , 2001, Cerebral cortex.

[35]  O. Spreen,et al.  A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary , 1991 .

[36]  Alan C. Evans,et al.  Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. , 1996, Cerebral cortex.

[37]  A M Owen,et al.  Double dissociations of memory and executive functions in working memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. , 1996, Brain : a journal of neurology.

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

[39]  B. Vogt,et al.  Human cingulate cortex: Surface features, flat maps, and cytoarchitecture , 1995, The Journal of comparative neurology.

[40]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[41]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[42]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[43]  Alan C. Evans,et al.  In vivo morphometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior‐rostral sulci: Hemispheric asymmetries, gender differences and probability maps , 1996, The Journal of comparative neurology.

[44]  K Y Liang,et al.  Longitudinal data analysis for discrete and continuous outcomes. , 1986, Biometrics.

[45]  M. Botvinick,et al.  Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  A Baddeley,et al.  The fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Jonathan D. Cohen,et al.  Dissociating working memory from task difficulty in human prefrontal cortex , 1997, Neuropsychologia.

[48]  H. Breiter,et al.  A functional magnetic resonance imaging study of auditory vigilance with low and high information processing demands. , 1998, Neuropsychology.

[49]  E J Auerbach,et al.  Activity in the paracingulate and cingulate sulci during word generation: an fMRI study of functional anatomy. , 1999, Cerebral cortex.

[50]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[51]  N. J. Herrod,et al.  Redefining the functional organization of working memory processes within human lateral prefrontal cortex , 1999, The European journal of neuroscience.

[52]  R. Dolan,et al.  Neural systems engaged by planning: a PET study of the Tower of London task , 1996, Neuropsychologia.