Selective activation of the superior frontal gyrus in task-switching: An event-related fNIRS study

In the task-switching paradigm, reaction time is longer and accuracy is worse in switch trials relative to repetition trials. This so-called switch cost has been ascribed to the engagement of control processes required to alternate between distinct stimulus-response mapping rules. Neuroimaging studies have reported an enhanced activation of the human lateral prefrontal cortex and the superior frontal gyrus during the task-switching paradigm. Whether neural activation in these regions is dissociable and associated with separable cognitive components of task switching has been a matter of recent debate. We used multi-channel near-infrared spectroscopy (fNIRS) to measure brain cortical activity in a task-switching paradigm designed to avoid task differences, order predictability, and frequency effects. The results showed a generalized bilateral activation of the lateral prefrontal cortex and the superior frontal gyrus in both switch trials and repetition trials. To isolate the activity selectively associated with the task-switch, the overall activity recorded during repetition trials was subtracted from the activity recorded during switch trials. Following subtraction, the remaining activity was entirely confined to the left portion of the superior frontal gyrus. The present results suggest that factors associated with load and maintenance of distinct stimulus-response mapping rules in working memory are likely contributors to the activation of the lateral prefrontal cortex, whereas only activity in the left superior frontal gyrus can be linked unequivocally to switching between distinct cognitive tasks.

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

[2]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[3]  D. Delpy,et al.  System for long-term measurement of cerebral blood and tissue oxygenation on newborn infants by near infra-red transillumination , 1988, Medical and Biological Engineering and Computing.

[4]  N. Meiran.  Reconfiguration of processing mode prior to task performance. , 1996 .

[5]  Archana K. Singh,et al.  Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI , 2005, NeuroImage.

[6]  Frithjof Kruggel,et al.  Age dependency of the hemodynamic response as measured by functional near-infrared spectroscopy , 2003, NeuroImage.

[7]  Masako Okamoto,et al.  Automated cortical projection of head-surface locations for transcranial functional brain mapping , 2005, NeuroImage.

[8]  T. Bussey,et al.  Role of prefrontal cortex in a network for arbitrary visuomotor mapping , 2000, Experimental Brain Research.

[9]  E. Gratton,et al.  On-line optical imaging of the human brain with 160-ms temporal resolution. , 2000, Optics express.

[10]  A. Dove,et al.  Prefrontal cortex activation in task switching: an event-related fMRI study. , 2000, Brain research. Cognitive brain research.

[11]  D. Alan Allport,et al.  SHIFTING INTENTIONAL SET - EXPLORING THE DYNAMIC CONTROL OF TASKS , 1994 .

[12]  Franca Stablum,et al.  Multitasking costs in close-head injury patients , 2003, Experimental Brain Research.

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

[14]  K. A. Hadland,et al.  Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. , 2002, Journal of neurophysiology.

[15]  K. Kubota,et al.  Cortical Mapping of Gait in Humans: A Near-Infrared Spectroscopic Topography Study , 2001, NeuroImage.

[16]  N. Yeung,et al.  Switching between tasks of unequal familiarity: the role of stimulus-attribute and response-set selection. , 2003, Journal of experimental psychology. Human perception and performance.

[17]  J. Lancaster,et al.  Using the talairach atlas with the MNI template , 2001, NeuroImage.

[18]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of response modality and processing domain. , 2001, Cerebral Cortex.

[19]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[20]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[21]  Archana K. Singh,et al.  Exploring the false discovery rate in multichannel NIRS , 2006, NeuroImage.

[22]  Frithjof Kruggel,et al.  Near‐infrared spectroscopy can detect brain activity during a color–word matching Stroop task in an event‐related design , 2002, Human brain mapping.

[23]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[24]  Arthur F. Kramer,et al.  Strategies and automaticity. I: Basic findings and conceptual framework , 1994 .

[25]  T. Robbins,et al.  Dissociating executive mechanisms of task control following frontal lobe damage and Parkinson's disease. , 1998, Brain : a journal of neurology.

[26]  S. Monsell.  Task switching , 2003, Trends in Cognitive Sciences.

[27]  D. Meyer,et al.  Executive control of cognitive processes in task switching. , 2001, Journal of experimental psychology. Human perception and performance.

[28]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[29]  R. Passingham,et al.  Learning Arbitrary Visuomotor Associations: Temporal Dynamic of Brain Activity , 2001, NeuroImage.

[30]  D. Manoach,et al.  Prefrontal cortex fMRI signal changes are correlated with working memory load , 1997, Neuroreport.

[31]  M. Moscovitch,et al.  Attention and Performance 15: Conscious and Nonconscious Information Processing , 1994 .

[32]  A. Villringer,et al.  Non-invasive optical spectroscopy and imaging of human brain function , 1997, Trends in Neurosciences.

[33]  A. A. Wijers,et al.  An event-related brain potential correlate of visual short-term memory. , 1999, Neuroreport.

[34]  Ivan Toni,et al.  Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study , 1999, Experimental Brain Research.

[35]  N. Meiran,et al.  Component Processes in Task Switching , 2000, Cognitive Psychology.

[36]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[37]  D Gopher,et al.  Switching tasks and attention policies. , 2000, Journal of experimental psychology. General.

[38]  M. Tamura,et al.  Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. , 2001, Journal of applied physiology.

[39]  S Nioka,et al.  Quantitation of time- and frequency-resolved optical spectra for the determination of tissue oxygenation. , 1991, Analytical biochemistry.

[40]  M. Brass,et al.  The role of the frontal cortex in task preparation. , 2002, Cerebral cortex.

[41]  K. Arbuthnott,et al.  Executive control in set switching: residual switch cost and task-set inhibition. , 2000, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[42]  D. Delpy,et al.  Measurement of Cranial Optical Path Length as a Function of Age Using Phase Resolved Near Infrared Spectroscopy , 1994 .

[43]  Jordan Grafman,et al.  The Roles of Timing and Task Order during Task Switching , 2002, NeuroImage.

[44]  P. Lachenbruch.  Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[45]  D. Boas,et al.  Non-invasive neuroimaging using near-infrared light , 2002, Biological Psychiatry.

[46]  K. Izzetoglu,et al.  Registering fNIR Data to Brain Surface Image using MRI templates , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[47]  Hellmuth Obrig,et al.  Towards a standard analysis for functional near-infrared imaging , 2004, NeuroImage.

[48]  G. Taga,et al.  Brain imaging in awake infants by near-infrared optical topography , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[49]  R Dell'Acqua,et al.  Spatial attention freezes during the attention blink. , 2006, Psychophysiology.

[50]  B. Hommel,et al.  Task-switching and long-term priming: Role of episodic stimulus–task bindings in task-shift costs , 2003, Cognitive Psychology.

[51]  R. A. Carlson,et al.  Effects of repetition and foreknowledge in task-set reconfiguration. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[52]  J. Grafman,et al.  Dissociating the roles of the rostral anterior cingulate and the lateral prefrontal cortices in performing two tasks simultaneously or successively. , 2003, Cerebral cortex.

[53]  G. Mangun,et al.  Brain regions activated by endogenous preparatory set shifting as revealed by fMRI , 2006, Cognitive, affective & behavioral neuroscience.

[54]  A Baddeley,et al.  Random Generation and the Executive Control of Working Memory , 1998, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[55]  M. D’Esposito,et al.  Modulation of task-related neural activity in task-switching: an fMRI study. , 2000, Brain research. Cognitive brain research.

[56]  Yoko Hoshi,et al.  Spatiotemporal characteristics of hemodynamic changes in the human lateral prefrontal cortex during working memory tasks , 2003, NeuroImage.

[57]  John R. Anderson,et al.  The role of prefrontal cortex and posterior parietal cortex in task switching. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[58]  D Y von Cramon,et al.  Executive control functions in task switching: evidence from brain injured patients. , 1999, Journal of clinical and experimental neuropsychology.

[59]  Kazuo Hiraki,et al.  Decrease in prefrontal hemoglobin oxygenation during reaching tasks with delayed visual feedback: a near-infrared spectroscopy study. , 2004, Brain research. Cognitive brain research.

[60]  D. Yves von Cramon,et al.  Neurovascular coupling is impaired in cerebral microangiopathy—An event-related Stroop study , 2007, NeuroImage.

[61]  D. Stuss,et al.  Wisconsin Card Sorting Test performance in patients with focal frontal and posterior brain damage: effects of lesion location and test structure on separable cognitive processes , 2000, Neuropsychologia.

[62]  K. Sakai,et al.  Temporal cortex activation during speech recognition: an optical topography study , 1999, Cognition.

[63]  David A. Boas,et al.  Evidence that cerebral blood volume can provide brain activation maps with better spatial resolution than deoxygenated hemoglobin , 2005, NeuroImage.

[64]  E. Miller,et al.  Neural circuits subserving the retrieval and maintenance of abstract rules. , 2003, Journal of neurophysiology.

[65]  I. Oda,et al.  Variation of temporal characteristics in human cerebral hemodynamic responses to electric median nerve stimulation: a near-infrared spectroscopic study , 2001, Neuroscience Letters.

[66]  Harold Pashler,et al.  A neuropsychological assessment of dual-task costs in closed-head injury patients using Cohen’s effect size estimation method , 2006, Psychological research.

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

[68]  Mark D'Esposito,et al.  Selection and maintenance of stimulus–response rules during preparation and performance of a spatial choice-reaction task , 2007, Brain Research.

[69]  T. Braver,et al.  Anterior Cingulate Cortex and Response Conflict : Effects of Response Modality and Processing Domain , 2022 .

[70]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[71]  K. Berman,et al.  Fractionating the neural substrate of cognitive control processes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[72]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[73]  M. Schmitter-Edgecombe,et al.  Costs of a predictable switch between simple cognitive tasks following severe closed-head injury. , 2006, Neuropsychology.

[74]  S. Keele,et al.  Changing internal constraints on action: the role of backward inhibition. , 2000, Journal of experimental psychology. General.