Functional MRI investigation of verbal selection mechanisms in lateral prefrontal cortex

Response selection activates appropriate response representations to task-relevant environmental stimuli. Research implicates dorsolateral prefrontal cortex (dlPFC) for this process. On the other hand, studies of semantic selection, which activates verbal responses based on the semantic requirements of a task, implicate ventrolateral PFC (vlPFC). Despite this apparent dissociation, the neurocognitive distinction between response and semantic selection is controversial. The current functional MRI study attempts to resolve this controversy by investigating verbal response and semantic selection in the same participants. Participants responded vocally with a word to a visually presented noun, either from a memorized list of paired associates (response selection task), or by generating a semantically related verb (semantic selection task). We found a dissociation in left lateral PFC. Activation increased significantly in dlPFC with response selection difficulty, but not semantic selection difficulty. Conversely, semantic, but not response, selection difficulty increased activity significantly in vlPFC. Activity in left parietal cortex, on the other hand, was affected by difficulty increases in both selection tasks. These results suggest that response and semantic selection may be distinct cognitive processes mediated by different regions of lateral PFC; but both of these selection processes rely on cognitive mechanisms mediated by parietal cortex.

[1]  Douglas C. Noll,et al.  Overt Verbal Responding during fMRI Scanning: Empirical Investigations of Problems and Potential Solutions , 1999, NeuroImage.

[2]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[3]  N. Kanwisher,et al.  Common Neural Substrates for Response Selection across Modalities and Mapping Paradigms , 2003, Journal of Cognitive Neuroscience.

[4]  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.

[5]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[6]  R. Remington,et al.  The role of input and output modality pairings in dual-task performance: Evidence for content-dependent central interference , 2006, Cognitive Psychology.

[7]  D. Manoach Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings , 2003, Schizophrenia Research.

[8]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[9]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[10]  Eric H. Schumacher,et al.  Sustained involvement of a frontal–parietal network for spatial response selection with practice of a spatial choice–reaction task , 2005, Neuropsychologia.

[11]  D E Kieras,et al.  A computational theory of executive cognitive processes and multiple-task performance: Part 1. Basic mechanisms. , 1997, Psychological review.

[12]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[13]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

[14]  Carol L. Colby,et al.  Stimulus–Response Incompatibility Activates Cortex Proximate to Three Eye Fields , 2001, NeuroImage.

[15]  Eliot Hazeltine,et al.  Simultaneous dual-task performance reveals parallel response selection after practice. , 2002, Journal of experimental psychology. Human perception and performance.

[16]  Sharon L. Thompson-Schill,et al.  Prefrontal Cortical Response to Conflict during Semantic and Phonological Tasks , 2007, Journal of Cognitive Neuroscience.

[17]  M. D’Esposito,et al.  The neural effect of stimulus-response modality compatibility on dual-task performance: an fMRI study , 2006, Psychological research.

[18]  Mark D'Esposito,et al.  Neural mechanisms for response selection: comparing selection of responses and items from working memory , 2007, NeuroImage.

[19]  John D. E. Gabrieli,et al.  Material-dependent and material-independent selection processes in the frontal and parietal lobes: an event-related fMRI investigation of response competition , 2003, Neuropsychologia.

[20]  P. Fletcher,et al.  Selecting among competing alternatives: selection and retrieval in the left inferior frontal gyrus. , 2005, Cerebral cortex.

[21]  Irene P. Kan,et al.  Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Walter Schneider,et al.  Controlled & automatic processing: behavior, theory, and biological mechanisms , 2003, Cogn. Sci..

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

[24]  Peter A. Bandettini,et al.  Experimental designs and processing strategies for fMRI studies involving overt verbal responses , 2004, NeuroImage.

[25]  Jia-Hong Gao,et al.  Is left inferior frontal gyrus a general mechanism for selection? , 2004, NeuroImage.

[26]  R. Buckner,et al.  Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups. , 1995, Journal of neurophysiology.

[27]  A. Wagner,et al.  Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. , 2005, Cerebral cortex.

[28]  E. Auerbach,et al.  Relative Shift in Activity from Medial to Lateral Frontal Cortex During Internally Versus Externally Guided Word Generation , 2001, Journal of Cognitive Neuroscience.

[29]  Irene P. Kan,et al.  Effects of Repetition and Competition on Activity in Left Prefrontal Cortex during Word Generation , 1999, Neuron.

[30]  James B. Rowe,et al.  Working Memory for Location and Time: Activity in Prefrontal Area 46 Relates to Selection Rather than Maintenance in Memory , 2001, NeuroImage.

[31]  A. Osman,et al.  Dimensional overlap: cognitive basis for stimulus-response compatibility--a model and taxonomy. , 1990, Psychological review.

[32]  T. Shallice,et al.  “Sculpting the Response Space”—An Account of Left Prefrontal Activation at Encoding , 2000, NeuroImage.

[33]  A. Braun,et al.  Comparison of continuous overt speech fMRI using BOLD and arterial spin labeling , 2005, Human brain mapping.

[34]  Jennifer M. Glass,et al.  Concurrent response-selection processes in dual-task performance: Evidence for adaptive executive control of task scheduling. , 1999 .

[35]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[37]  Jennifer M. Glass,et al.  Virtually Perfect Time Sharing in Dual-Task Performance: Uncorking the Central Cognitive Bottleneck , 2001, Psychological science.

[38]  H. Pashler Dual-task interference in simple tasks: data and theory. , 1994, Psychological bulletin.

[39]  Karl J. Friston,et al.  The prefrontal cortex shows context-specific changes in effective connectivity to motor or visual cortex during the selection of action or colour. , 2004, Cerebral cortex.

[40]  Irene P. Kan,et al.  Selection from perceptual and conceptual representations , 2004, Cognitive, affective & behavioral neuroscience.

[41]  M. Petrides The role of the mid-dorsolateral prefrontal cortex in working memory , 2000, Experimental Brain Research.

[42]  E C Wong,et al.  Effect of motion outside the field of view on functional MR. , 1996, AJNR. American journal of neuroradiology.

[43]  M. D’Esposito,et al.  Neural Evidence for Representation-Specific Response Selection , 2003, Journal of Cognitive Neuroscience.

[44]  D. Schacter,et al.  Prefrontal Contributions to Executive Control: fMRI Evidence for Functional Distinctions within Lateral Prefrontal Cortex , 2001, NeuroImage.

[45]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[46]  M. D’Esposito,et al.  Neural implementation of response selection in humans as revealed by localized effects of stimulus–response compatibility on brain activation , 2002, Human brain mapping.

[47]  J. Fiez,et al.  Using neuroimaging to evaluate models of working memory and their implications for language processing , 2003, Journal of Neurolinguistics.

[48]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

[49]  Vincent L. Gracco,et al.  Contribution of the frontal lobe to externally and internally specified verbal responses: fMRI evidence , 2006, NeuroImage.

[50]  Edward E. Smith,et al.  Verbal Working Memory Load Affects Regional Brain Activation as Measured by PET , 1997, Journal of Cognitive Neuroscience.

[51]  E Zarahn,et al.  Event-related functional MRI: implications for cognitive psychology. , 1999, Psychological bulletin.

[52]  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..

[53]  J. Jonides,et al.  Brain mechanisms of proactive interference in working memory , 2006, Neuroscience.

[54]  R W Cox,et al.  Magnetic field changes in the human brain due to swallowing or speaking , 1998, Magnetic resonance in medicine.

[55]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.