Skip to main content

Advertisement

Log in

Architecture of fluid intelligence and working memory revealed by lesion mapping

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ackerman PL, Beier ME, Boyle MO (2002) Individual differences in working memory within a nomological network of cognitive and perceptual speed abilities. J Exp Psychol Gen 131:567–589

    Article  PubMed  Google Scholar 

  • Baldo JV, Dronkers NF (2006) The role of inferior parietal and inferior frontal cortex in working memory. Neuropsychology 20:529–538

    Article  PubMed  Google Scholar 

  • Barbey AK, Krueger F, Grafman J (2009) An evolutionarily adaptive neural architecture for social reasoning. Trends Neurosci 32:603–610

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barbey AK, Koenigs M, Grafman J (2011) Orbitofrontal contributions to human working memory. Cereb Cortex 21:789–795

    Article  PubMed  Google Scholar 

  • Barbey AK, Colom R, Solomon J, Krueger F, Forbes C, Grafman J (2012a) An integrative architecture for general intelligence and executive function revealed by lesion mapping. Brain 135:1154–1164

    Article  PubMed  Google Scholar 

  • Barbey AK, Koenigs M, Grafman J (2012b) Dorsolateral prefrontal contributions to human working memory. Cortex (epub ahead of print)

  • Barbey AK, Colom R, Grafman J (2012c) Distributed neural system for emotional intelligence revealed by lesion mapping. Soc Cogn Affect Neurosci (epub ahead of print)

  • Basso A, De Renzi E, Faglioni P, Scotti G, Spinnler H (1973) Neuropsychological evidence for the existence of cerebral areas critical to the performance of intelligence tasks. Brain 96:715–728

    Article  CAS  PubMed  Google Scholar 

  • Bates E, Wilson SM, Saygin AP, Dick F, Sereno MI, Knight RT, Dronkers NF (2003) Voxel-based lesion-symptom mapping. Nat Neurosci 6:448–450

    CAS  PubMed  Google Scholar 

  • Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50:7–15

    Article  CAS  PubMed  Google Scholar 

  • Bennett CM, Miller MB (2010) How reliable are the results from functional magnetic resonance imaging? Ann N Y Acad Sci 1191:133–155

    Article  PubMed  Google Scholar 

  • Black FW (1976) Cognitive deficits in patients with unilateral war-related frontal lobe lesions. J Clin Psychol 32:366–372

    Article  CAS  PubMed  Google Scholar 

  • Blair RJ, Cipolotti L (2000) Impaired social response reversal. A case of ‘acquired sociopathy’. Brain 123(Pt 6):1122–1141

    Article  PubMed  Google Scholar 

  • Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Psychol Rev 108:624–652

    Article  CAS  PubMed  Google Scholar 

  • Bugg JM, Zook NA, Delosh EL, Davalos DB, Davis HP (2006) Age differences in fluid intelligence: contributions of general slowing and frontal decline. Brain Cogn 62:9–16

    Article  PubMed  Google Scholar 

  • Burgess PW, Shallice T (1996) Response suppression, initiation and strategy use following frontal lobe lesions. Neuropsychologia 34:263–272

    Article  CAS  PubMed  Google Scholar 

  • Carroll JB (1993) Human cognitive abilities: a survey of factor-analytic studies. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Cattell RB (1971) Abilities: their structure, growth, and action. Houghton Mifflin, Boston

    Google Scholar 

  • Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE (1997) Temporal dynamics of brain activation during a working memory task. Nature 386:604–608

    Article  CAS  PubMed  Google Scholar 

  • Colom R, Rebollo I, Palacios A, Juan-Espinosa M, Kyllonen PC (2004) Working memory is (almost) perfectly predicted by g. Intelligence 32:277–296

    Article  Google Scholar 

  • Colom R, Abad FJ, Rebollo I, Shih PC (2005) Memory span and general intelligence: a latent-variable approach. Intelligence 33:623–642

    Article  Google Scholar 

  • Colom R, Jung RE, Haier RJ (2007) General intelligence and memory span: evidence for a common neuroanatomic framework. Cogn Neuropsychol 24:867–878

    Article  PubMed  Google Scholar 

  • Colom R, Haier RJ, Head K, Alvarez-Linera J, Quiroga MA, Shih PC, Jung RE (2009) Gray matter correlates of fluid, crystallized, and spatial intelligence: testing the P-FIT model. Intelligence 37:124–135

    Article  Google Scholar 

  • Crone EA, Wendelken C, Donohue SE, Bunge SA (2006) Neural evidence for dissociable components of task-switching. Cereb Cortex 16:475–486

    Article  PubMed  Google Scholar 

  • D’esposito M, Postle BR (1999) The dependence of span and delayed-response performance on prefrontal cortex. Neuropsychologia 37:1303–1315

    Article  PubMed  Google Scholar 

  • D’esposito M, Cooney JW, Gazzaley A, Gibbs SE, Postle BR (2006) Is the prefrontal cortex necessary for delay task performance? Evidence from lesion and FMRI data. J Int Neuropsychol Soc 12:248–260

    PubMed  Google Scholar 

  • Dosenbach NU, Visscher KM, Palmer ED, Miezin FM, Wenger KK, Kang HC, Burgund ED, Grimes AL, Schlaggar BL, Petersen SE (2006) A core system for the implementation of task sets. Neuron 50:799–812

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Duncan J (2001) An adaptive coding model of neural function in prefrontal cortex. Nat Rev Neurosci 2:820–829

    Article  CAS  PubMed  Google Scholar 

  • Duncan J (2010) The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn Sci 14:172–179

    Article  PubMed  Google Scholar 

  • Duncan J, Burgess P, Emslie H (1995) Fluid intelligence after frontal lobe lesions. Neuropsychologia 33:261–268

    Article  CAS  PubMed  Google Scholar 

  • Duncan J, Emslie H, Williams P, Johnson R, Freer C (1996) Intelligence and the frontal lobe: the organization of goal-directed behavior. Cogn Psychol 30:257–303

    Article  CAS  PubMed  Google Scholar 

  • Eslinger PJ, Damasio AR (1985) Severe disturbance of higher cognition after bilateral frontal lobe ablation: patient EVR. Neurology 35:1731–1741

    Article  CAS  PubMed  Google Scholar 

  • Glascher J, Tranel D, Paul LK, Rudrauf D, Rorden C, Hornaday A, Grabowski T, Damasio H, Adolphs R (2009) Lesion mapping of cognitive abilities linked to intelligence. Neuron 61:681–691

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Glascher J, Rudrauf D, Colom R, Paul LK, Tranel D, Damasio H, Adolphs R (2010) Distributed neural system for general intelligence revealed by lesion mapping. Proc Natl Acad Sci USA 107:4705–4709

    Article  CAS  PubMed  Google Scholar 

  • Gray JR, Chabris CF, Braver TS (2003) Neural mechanisms of general fluid intelligence. Nat Neurosci 6:316–322

    Article  CAS  PubMed  Google Scholar 

  • Haier RJ, Colom R, Schroeder DH, Condon CA, Tang C, Eaves E, Head K (2009) Gray matter and intelligence factors: is there a neurology? Intelligence 37:136–144

    Article  Google Scholar 

  • Isingrini M, Vazou F (1997) Relation between fluid intelligence and frontal lobe functioning in older adults. Int J Aging Hum Dev 45:99–109

    Article  CAS  PubMed  Google Scholar 

  • Jaeggi SM, Buschkuehl M, Jonides J, Perrig WJ (2008) Improving fluid intelligence with training on working memory. Proc Natl Acad Sci USA 105:6829–6833

    Article  CAS  PubMed  Google Scholar 

  • Jaeggi SM, Studer-Luethi B, Buschkuehl M, Su YF, Jonides J, Perrig WJ (2010) The relationship between n-back performance and matrix reasoning—implications for training and transfer. Intelligence 38:625–635

    Article  Google Scholar 

  • Jaeggi SM, Buschkuehl M, Jonides J, Shah P (2011) Short- and long-term benefits of cognitive training. Proc Natl Acad Sci USA 108:10081–10086

    Article  CAS  PubMed  Google Scholar 

  • Jensen AR (1998) The g factor: the science of mental ability. Praeger, Westport, Conn

    Google Scholar 

  • Johnson W, Bouchard TJ (2005) The structure of human intelligence: it is verbal, perceptual, and image rotation (VPR), not fluid and crystallized. Intelligence 33:393–416

    Article  Google Scholar 

  • Jung RE, Haier RJ (2007) The Parieto-Frontal Integration Theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 30:135–154 (discussion 154–187)

    Article  PubMed  Google Scholar 

  • Kane MJ, Engle RW (2002) The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: an individual-differences perspective. Psychon Bull Rev 9:637–671

    Article  PubMed  Google Scholar 

  • Karama S, Colom R, Johnson W, Deary IJ, Haier R, Waber DP, Lepage C, Ganjavi H, Jung R, Evans AC (2011) Cortical thickness correlates of specific cognitive performance accounted for by the general factor of intelligence in healthy children aged 6 to 18. Neuroimage 55:1443–1453

    Article  PubMed Central  PubMed  Google Scholar 

  • Koechlin E, Basso G, Pietrini P, Panzer S, Grafman J (1999) The role of the anterior prefrontal cortex in human cognition. Nature 399:148–151

    Article  CAS  PubMed  Google Scholar 

  • Koenigs M, Barbey AK, Postle BR, Grafman J (2009) Superior parietal cortex is critical for the manipulation of information in working memory. J Neurosci 29:14980–14986

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kroger JK, Sabb FW, Fales CL, Bookheimer SY, Cohen MS, Holyoak KJ (2002) Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: a parametric study of relational complexity. Cereb Cortex 12:477–485

    Article  PubMed  Google Scholar 

  • Kyllonen PC, Christal RE (1990) Reasoning ability is (little more than) working-memory capacity. Intelligence 14:389–433

    Article  Google Scholar 

  • Makale M, Solomon J, Patronas NJ, Danek A, Butman JA, Grafman J (2002) Quantification of brain lesions using interactive automated software. Behav Res Methods Instr Comput 34:6–18

    Article  Google Scholar 

  • Martinez K, Burgaleta M, Roman FJ, Escorial S, Shih PC, Quiroga MA, Colom R (2011) Can fluid intelligence be reduced to ‘simple’ short-term storage? Intelligence 39:473–480

    Article  Google Scholar 

  • Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202

    Article  CAS  PubMed  Google Scholar 

  • Muller NG, Machado L, Knight RT (2002) Contributions of subregions of the prefrontal cortex to working memory: evidence from brain lesions in humans. J Cogn Neurosci 14:673–686

    Article  PubMed  Google Scholar 

  • Nyberg L, Marklund P, Persson J, Cabeza R, Forkstam C, Petersson KM, Ingvar M (2003) Common prefrontal activations during working memory, episodic memory, and semantic memory. Neuropsychologia 41:371–377

    Article  PubMed  Google Scholar 

  • Parkin AJ, Java RI (1999) Deterioration of frontal lobe function in normal aging: influences of fluid intelligence versus perceptual speed. Neuropsychology 13:539–545

    Article  CAS  PubMed  Google Scholar 

  • Ramnani N, Owen AM (2004) Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci 5:184–194

    Article  CAS  PubMed  Google Scholar 

  • Raymont V, Salazar AM, Lipsky R, Goldman D, Tasick G, Grafman J (2010) Correlates of posttraumatic epilepsy 35 years following combat brain injury. Neurology 75:224–229

    Article  CAS  PubMed  Google Scholar 

  • Roca M, Parr A, Thompson R, Woolgar A, Torralva T, Antoun N, Manes F, Duncan J (2010) Executive function and fluid intelligence after frontal lobe lesions. Brain 133:234–247

    Article  PubMed  Google Scholar 

  • Rombouts SA, Barkhof F, Hoogenraad FG, Sprenger M, Valk J, Scheltens P (1997) Test-retest analysis with functional MR of the activated area in the human visual cortex. AJNR Am J Neuroradiol 18:1317–1322

    CAS  PubMed  Google Scholar 

  • Semendeferi K, Armstrong E, Schleicher A, Zilles K, Van Hoesen GW (2001) Prefrontal cortex in humans and apes: a comparative study of area 10. Am J Phys Anthropol 114:224–241

    Article  CAS  PubMed  Google Scholar 

  • Shallice T, Burgess PW (1991) Deficits in strategy application following frontal lobe damage in man. Brain 114(Pt 2):727–741

    Article  PubMed  Google Scholar 

  • Solomon J, Raymont V, Braun A, Butman JA, Grafman J (2007) User-friendly software for the analysis of brain lesions (ABLe). Comput Methods Progr Biomed 86:245–254

    Article  Google Scholar 

  • Spearman C (1904) “General intelligence” objectively determined and measured. Am J Psychol 15:201–292

    Article  Google Scholar 

  • Spearman C (1928) The abilities of man. Science 68:38

    Article  CAS  PubMed  Google Scholar 

  • Suss HM, Oberauer K, Wittmann WW, Wilhelm O, Schulze R (2002) Working-memory capacity explains reasoning ability—and a little bit more. Intelligence 30:261–288

    Article  Google Scholar 

  • Tsuchida A, Fellows LK (2009) Lesion evidence that two distinct regions within prefrontal cortex are critical for n-back performance in humans. J Cogn Neurosci 21:2263–2275

    Article  PubMed  Google Scholar 

  • Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289

    Article  CAS  PubMed  Google Scholar 

  • Van Essen DC, Dierker DL (2007) Surface-based and probabilistic atlases of primate cerebral cortex. Neuron 56:209–225

    Article  PubMed  Google Scholar 

  • Volle E, Kinkingnehun S, Pochon JB, Mondon K, Thiebaut De Schotten M, Seassau M, Duffau H, Samson Y, Dubois B, Levy R (2008) The functional architecture of the left posterior and lateral prefrontal cortex in humans. Cerebral Cortex 18:2460–2469

    Article  PubMed  Google Scholar 

  • Wechsler D (1997) Wechsler adult intelligence test administration and scoring manual. The Psychology Corporation, San Antonio

    Google Scholar 

  • Woods RP, Mazziotta JC, Cherry SR (1993) MRI-PET registration with automated algorithm. J Comput Assist Tomogr 17:536–546

    Article  CAS  PubMed  Google Scholar 

  • Woolgar A, Parr A, Cusack R, Thompson R, Nimmo-Smith I, Torralva T, Roca M, Antoun N, Manes F, Duncan J (2010) Fluid intelligence loss linked to restricted regions of damage within frontal and parietal cortex. Proc Natl Acad Sci USA 107:14899–14902

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to S. Bonifant, B. Cheon, C. Ngo, A. Greathouse, V. Raymont, K. Reding, and G. Tasick for their invaluable help with the testing of participants and organization of this study. This work was supported by funding from the US National Institute of Neurological Disorders and Stroke intramural research program and a project grant from the United States Army Medical Research and Material Command administered by the Henry M. Jackson Foundation (Vietnam Head Injury Study Phase III: a 30-year post-injury follow-up study, grant number DAMD17-01-1-0675). R. Colom was supported by grant PSI2010-20364 from Ministerio de Ciencia e Innovación [Ministry of Science and Innovation, Spain].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aron K. Barbey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 104 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barbey, A.K., Colom, R., Paul, E.J. et al. Architecture of fluid intelligence and working memory revealed by lesion mapping. Brain Struct Funct 219, 485–494 (2014). https://doi.org/10.1007/s00429-013-0512-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-013-0512-z

Keywords

Navigation