Global Increase in Task-related Fronto-parietal Activity after Focal Frontal Lobe Lesion

A critical question for neuropsychology is how complex brain networks react to damage. Here, we address this question for the well-known executive control or multiple-demand (MD) system, a fronto-parietal network showing increased activity with many different kinds of cognitive demand, including standard tests of fluid intelligence. Using fMRI, we ask how focal frontal lobe damage affects MD activity during a standard fluid intelligence task. Despite poor behavioral performance, frontal patients showed increased fronto-parietal activity relative to controls. The activation difference was not accounted for by difference in IQ. Moreover, rather than specific focus on perilesional or contralesional cortex, additional recruitment was distributed throughout the MD regions and surrounding cortex and included parietal MD regions distant from the injury. The data suggest that, following local frontal lobe damage, there is a global compensatory recruitment of an adaptive and integrated fronto-parietal network.

[1]  Stephen M. Smith,et al.  Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. , 2002, Brain : a journal of neurology.

[2]  H. Nelson.  A Modified Card Sorting Test Sensitive to Frontal Lobe Defects , 1976, Cortex.

[3]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Applications , 2002, NeuroImage.

[4]  M. Corbetta,et al.  Neural correlates of recovery from aphasia after damage to left inferior frontal cortex , 2000, Neurology.

[5]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[6]  N. Ward,et al.  The neural substrates of motor recovery after focal damage to the central nervous system. , 2006, Archives of physical medicine and rehabilitation.

[7]  J. Duncan,et al.  Adaptive Coding of Task-Relevant Information in Human Frontoparietal Cortex , 2011, The Journal of Neuroscience.

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

[9]  M. Just,et al.  Plasticity of language-related brain function during recovery from stroke. , 1999, Stroke.

[10]  Kun Ho Lee,et al.  Neural correlates of superior intelligence: Stronger recruitment of posterior parietal cortex , 2006, NeuroImage.

[11]  J. Fuster,et al.  Mnemonic and predictive functions of cortical neurons in a memory task , 1992, Neuroreport.

[12]  L. Cohen,et al.  Functional imaging of intervention effects in stroke motor rehabilitation. , 2006, Archives of physical medicine and rehabilitation.

[13]  E. G. Jones.  Cerebral Cortex , 1987, Cerebral Cortex.

[14]  Walter Schneider,et al.  The cognitive control network: Integrated cortical regions with dissociable functions , 2007, NeuroImage.

[15]  William D. Marslen-Wilson,et al.  The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) study protocol: a cross-sectional, lifespan, multidisciplinary examination of healthy cognitive ageing , 2014, BMC Neurology.

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

[17]  Richard S. J. Frackowiak,et al.  Neural correlates of outcome after stroke: a cross-sectional fMRI study. , 2003, Brain : a journal of neurology.

[18]  M. Egan,et al.  Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. , 2003, The American journal of psychiatry.

[19]  Anthony Randal McIntosh,et al.  Towards a network theory of cognition , 2000, Neural Networks.

[20]  John Duncan,et al.  COMT val158met Genotype Affects Recruitment of Neural Mechanisms Supporting Fluid Intelligence , 2008, Cerebral cortex.

[21]  John Duncan,et al.  Discrete Object Representation, Attention Switching, and Task Difficulty in the Parietal Lobe , 2010, Journal of Cognitive Neuroscience.

[22]  A. Neubauer,et al.  Intelligence and neural efficiency , 2009, Neuroscience & Biobehavioral Reviews.

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

[24]  Karl J. Friston,et al.  Functional reorganization of the brain in recovery from striatocapsular infarction in man , 1992, Annals of neurology.

[25]  Mark D'Esposito,et al.  Focal Brain Lesions to Critical Locations Cause Widespread Disruption of the Modular Organization of the Brain , 2012, Journal of Cognitive Neuroscience.

[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]  M. Giese,et al.  Flexible Coding for Categorical Decisions in the Human Brain , 2007, The Journal of Neuroscience.

[28]  S. Black,et al.  Evidence from Functional Neuroimaging of a Compensatory Prefrontal Network in Alzheimer's Disease , 2003, The Journal of Neuroscience.

[29]  Silvia A. Bunge,et al.  Evolutionary and Developmental Changes in the Lateral Frontoparietal Network: A Little Goes a Long Way for Higher-Level Cognition , 2014, Neuron.

[30]  J. Duncan.  EPS Mid-Career Award 2004: Brain mechanisms of attention , 2006, Quarterly journal of experimental psychology.

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

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

[33]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[34]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Theory , 2002, NeuroImage.

[35]  David J. Freedman,et al.  Experience-dependent representation of visual categories in parietal cortex , 2006, Nature.

[36]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

[37]  Chris Rorden,et al.  Spatial Normalization of Brain Images with Focal Lesions Using Cost Function Masking , 2001, NeuroImage.

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

[39]  K. Uğurbil,et al.  Analysis of fMRI and finger tracking training in subjects with chronic stroke. , 2002, Brain : a journal of neurology.

[40]  D. A. Grant,et al.  A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. , 1948, Journal of experimental psychology.

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

[42]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

[43]  Gian Luca Romani,et al.  Differential patterns of cortical activation as a function of fluid reasoning complexity , 2009, Human brain mapping.