Architecture of fluid intelligence and working memory revealed by lesion mapping

Although cognitive neuroscience has made valuable progress in understanding the role of the prefrontal cortex in human intelligence, the functional networks that support adaptive behavior and novel problem solving remain to be well characterized. Here, we studied 158 human brain lesion patients to investigate the cognitive and neural foundations of key competencies for fluid intelligence and working memory. We administered a battery of neuropsychological tests, including the Wechsler Adult Intelligence Scale (WAIS) and the N-Back task. Latent variable modeling was applied to obtain error-free scores of fluid intelligence and working memory, followed by voxel-based lesion-symptom mapping to elucidate their neural substrates. The observed latent variable modeling and lesion results support an integrative framework for understanding the architecture of fluid intelligence and working memory and make specific recommendations for the interpretation and application of the WAIS and N-Back task to the study of fluid intelligence in health and disease.

[1]  J. Grafman,et al.  Distributed neural system for emotional intelligence revealed by lesion mapping. , 2014, Social cognitive and affective neuroscience.

[2]  Wm. R. Wright General Intelligence, Objectively Determined and Measured. , 1905 .

[3]  S. Rombouts,et al.  Test-retest analysis with functional MR of the activated area in the human visual cortex. , 1997, AJNR. American journal of neuroradiology.

[4]  Rex E. Jung,et al.  Cortical thickness correlates of specific cognitive performance accounted for by the general factor of intelligence in healthy children aged 6 to 18 , 2011, NeuroImage.

[5]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

[6]  A. Parkin,et al.  Deterioration of frontal lobe function in normal aging: influences of fluid intelligence versus perceptual speed. , 1999, Neuropsychology.

[7]  T. Shallice,et al.  Deficits in strategy application following frontal lobe damage in man. , 1991, Brain : a journal of neurology.

[8]  Jeffrey W. Cooney,et al.  Is the Prefrontal Cortex Necessary for Delay Task Performance? Evidence from Lesion and fMRI Data , 2006, Journal of the International Neuropsychological Society.

[9]  E. Crone,et al.  Neural evidence for dissociable components of task-switching. , 2006, Cerebral cortex.

[10]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[11]  Chris Rorden,et al.  Lesion Mapping of Cognitive Abilities Linked to Intelligence , 2009, Neuron.

[12]  Lesley K. Fellows,et al.  Lesion Evidence That Two Distinct Regions within Prefrontal Cortex are Critical for n-Back Performance in Humans , 2009, Journal of Cognitive Neuroscience.

[13]  Patrick C. Kyllonen,et al.  Reasoning ability is (little more than) working-memory capacity?! , 1990 .

[14]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

[15]  Cheuk Y. Tang,et al.  Gray Matter and Intelligence Factors: Is There a Neuro-g?. , 2009 .

[16]  J. Grafman,et al.  An evolutionarily adaptive neural architecture for social reasoning , 2009, Trends in Neurosciences.

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

[18]  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.

[19]  Michael B. Miller,et al.  How reliable are the results from functional magnetic resonance imaging? , 2010, Annals of the New York Academy of Sciences.

[20]  R. Cattell,et al.  Abilities : Their Structure , Growth , and Action , 2015 .

[21]  C. Spearman,et al.  "THE ABILITIES OF MAN". , 1928, Science.

[22]  Adrian Danek,et al.  Quantification of brain lesions using interactive automated software , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[23]  Chad E. Forbes,et al.  An integrative architecture for general intelligence and executive function revealed by lesion mapping. , 2012, Brain : a journal of neurology.

[24]  James K. Kroger,et al.  Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: a parametric study of relational complexity. , 2002, Cerebral cortex.

[25]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[26]  John Duncan,et al.  Fluid intelligence loss linked to restricted regions of damage within frontal and parietal cortex , 2010, Proceedings of the National Academy of Sciences.

[27]  Susanne M. Jaeggi,et al.  Improving fluid intelligence with training on working memory: a meta-analysis , 2008, Psychonomic Bulletin & Review.

[28]  J. Duncan,et al.  Intelligence and the Frontal Lobe: The Organization of Goal-Directed Behavior , 1996, Cognitive Psychology.

[29]  Michael C. Pyryt Human cognitive abilities: A survey of factor analytic studies , 1998 .

[30]  Thomas J. Bouchard,et al.  The structure of human intelligence: It is verbal, perceptual, and image rotation (VPR), not fluid and crystallized , 2005 .

[31]  Susanne M. Jaeggi,et al.  Short- and long-term benefits of cognitive training , 2011, Proceedings of the National Academy of Sciences.

[32]  Patrick C. Kyllonen,et al.  Working memory is (almost) perfectly predicted by g , 2004 .

[33]  L Cipolotti,et al.  Impaired social response reversal. A case of 'acquired sociopathy'. , 2000, Brain : a journal of neurology.

[34]  C. Chabris,et al.  Neural mechanisms of general fluid intelligence , 2003, Nature Neuroscience.

[35]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[36]  E. Renzi,et al.  Neuropsychological evidence for the existence of cerebral areas critical to the performance of intelligence tasks. , 1973, Brain : a journal of neurology.

[37]  Susanne M. Jaeggi,et al.  The Relationship between N-Back Performance and Matrix Reasoning--Implications for Training and Transfer. , 2010 .

[38]  Robert T. Knight,et al.  Contributions of Subregions of the Prefrontal Cortex to Working Memory: Evidence from Brain Lesions in Humans , 2002, Journal of Cognitive Neuroscience.

[39]  M. Isingrini,et al.  Relation between Fluid Intelligence and Frontal Lobe Functioning in Older Adults , 1997, International journal of aging & human development.

[40]  Francisco J. Abad,et al.  Memory span and general intelligence: A latent-variable approach , 2005 .

[41]  Aron K Barbey,et al.  Orbitofrontal contributions to human working memory. , 2011, Cerebral cortex.

[42]  A. Jensen,et al.  The g factor , 1996, Nature.

[43]  T. Shallice,et al.  Response suppression, initiation and strategy use following frontal lobe lesions , 1996, Neuropsychologia.

[44]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[45]  Roberto Colom,et al.  General intelligence and memory span: Evidence for a common neuroanatomic framework , 2007, Cognitive neuropsychology.

[46]  R. Haier,et al.  The Parieto-Frontal Integration Theory (P-FIT) of intelligence: Converging neuroimaging evidence , 2007, Behavioral and Brain Sciences.

[47]  J. Duncan The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[48]  B. Postle,et al.  Superior Parietal Cortex Is Critical for the Manipulation of Information in Working Memory , 2009, The Journal of Neuroscience.

[49]  J. Carroll Human Cognitive Abilities-a sur-vey of factor-analytic studies , 1993 .

[50]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

[51]  J. Mazziotta,et al.  MRI‐PET Registration with Automated Algorithm , 1993, Journal of computer assisted tomography.

[52]  Nina F Dronkers,et al.  The role of inferior parietal and inferior frontal cortex in working memory. , 2006, Neuropsychology.

[53]  J. Grafman,et al.  Dorsolateral prefrontal contributions to human working memory , 2013, Cortex.

[54]  D. Goldman,et al.  Correlates of posttraumatic epilepsy 35 years following combat brain injury , 2010, Neurology.

[55]  J. Duncan,et al.  Fluid intelligence after frontal lobe lesions , 1995, Neuropsychologia.

[56]  Ralf Schulze,et al.  Working-memory capacity explains reasoning abilityand a little bit more , 2002 .

[57]  R. Engle,et al.  The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: An individual-differences perspective , 2002, Psychonomic bulletin & review.

[58]  D. V. Essen,et al.  Surface-Based and Probabilistic Atlases of Primate Cerebral Cortex , 2007, Neuron.

[59]  Allen R. Braun,et al.  User-friendly software for the analysis of brain lesions (ABLe) , 2007, Comput. Methods Programs Biomed..

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

[61]  Jonas Persson,et al.  Common prefrontal activations during working memory, episodic memory, and semantic memory , 2003, Neuropsychologia.

[62]  F. Black Cognitive deficits in patients with unilateral war-related frontal lobe lesions. , 1976, Journal of clinical psychology.

[63]  Kenia Martínez,et al.  Can fluid intelligence be reduced to 'simple' short-term storage? , 2011 .

[64]  D Rudrauf,et al.  Distributed neural system for general intelligence revealed by lesion mapping , 2010, Proceedings of the National Academy of Sciences.

[65]  John Duncan,et al.  Executive function and fluid intelligence after frontal lobe lesions , 2009, Brain : a journal of neurology.

[66]  Deana B. Davalos,et al.  Age differences in fluid intelligence: Contributions of general slowing and frontal decline , 2006, Brain and Cognition.

[67]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[68]  A A Bless A MCLEOD GAUGE OF WIDE RANGE. , 1928, Science.

[69]  Rex E. Jung,et al.  Gray matter correlates of fluid, crystallized, and spatial intelligence: Testing the P-FIT model , 2009 .

[70]  P. Ackerman,et al.  Individual differences in working memory within a nomological network of cognitive and perceptual speed abilities. , 2002, Journal of experimental psychology. General.

[71]  H. Duffau,et al.  The functional architecture of the left posterior and lateral prefrontal cortex in humans. , 2007, Cerebral cortex.

[72]  A. Damasio,et al.  Severe disturbance of higher cognition after bilateral frontal lobe ablation , 1985, Neurology.

[73]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.