Selective Retrieval of Abstract Semantic Knowledge in Left Prefrontal Cortex

Research into the representation and processing of conceptual knowledge has typically associated perceptual facts with sensory brain regions and executive retrieval mechanisms with the left prefrontal cortex. However, this dichotomy between knowledge content and retrieval processes leaves unanswered how the brain supports concepts less reliant on direct sensory experiences. We used neuroimaging methods to investigate whether an increased abstractness in semantic decisions, in contrast to increased response difficulty, is associated with increased left prefrontal activation. Participants were presented with concrete animal names and asked to verify sensory and abstract properties that corresponded only to the animal category. Candidate semantic regions were localized in left inferior, frontopolar, and dorsolateral prefrontal cortex in contrast to a pseudoword control. Activity in each of these prefrontal regions was associated with significantly increased activity for abstract relative to sensory semantic decisions, regardless of increased response difficulty and even when controlling for the response times of participants. These results suggest that more abstract, or verbally-mediated, semantic knowledge of concrete items, in contrast to more sensory-based properties, is specifically supported by the left prefrontal cortex. Semantic retrieval mechanisms may rely on abstract representations, likely coded through a verbal format, to mediate task demands when perceptual information is insufficient.

[1]  Jonathan D. Cohen,et al.  Prefrontal cortex and flexible cognitive control: rules without symbols. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Randy L Buckner,et al.  Common and dissociable activation patterns associated with controlled semantic and phonological processing: evidence from FMRI adaptation. , 2005, Cerebral cortex.

[3]  L. Barsalou,et al.  Situating Abstract Concepts , 2004 .

[4]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[5]  W. Schneider,et al.  Perceptual Knowledge Retrieval Activates Sensory Brain Regions , 2006, The Journal of Neuroscience.

[6]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[8]  Alex Martin,et al.  Functional Neuroimaging of Semantic Memory , 2001 .

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

[10]  S. Bunge How we use rules to select actions: A review of evidence from cognitive neuroscience , 2004, Cognitive, affective & behavioral neuroscience.

[11]  C. Price,et al.  Functional imaging of the semantic system: Retrieval of sensory-experienced and verbally learned knowledge , 2003, Brain and Language.

[12]  J. B. Demb,et al.  Semantic Repetition Priming for Verbal and Pictorial Knowledge: A Functional MRI Study of Left Inferior Prefrontal Cortex , 1997, Journal of Cognitive Neuroscience.

[13]  David Badre,et al.  Semantic retrieval, mnemonic control, and prefrontal cortex. , 2002, Behavioral and cognitive neuroscience reviews.

[14]  Lawrence W Barsalou,et al.  Abstraction in perceptual symbol systems. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.

[16]  L. Barsalou,et al.  Whither structured representation? , 1999, Behavioral and Brain Sciences.

[17]  Anthony D Wagner,et al.  Assembling and encoding word representations: fMRI subsequent memory effects implicate a role for phonological control , 2003, Neuropsychologia.

[18]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[19]  David Badre,et al.  Analogical reasoning and prefrontal cortex: evidence for separable retrieval and integration mechanisms. , 2004, Cerebral cortex.

[20]  E. Hoekendorf Hone your management skills for risk sharing. , 1997, Managed care strategies.

[21]  R. Buckner,et al.  Common Prefrontal Regions Coactivate with Dissociable Posterior Regions during Controlled Semantic and Phonological Tasks , 2002, Neuron.

[22]  C. Price,et al.  Retrieval of Visual, Auditory, and Abstract Semantics , 2002, NeuroImage.

[23]  W. Schneider,et al.  Distinct and common cortical activations for multimodal semantic categories , 2006, Cognitive, affective & behavioral neuroscience.

[24]  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.

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

[26]  M. McCloskey,et al.  Decision processes in verifying category membership statements: Implications for models of semantic memory , 1979, Cognitive Psychology.

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

[28]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[29]  P F Liddle,et al.  The role of the left prefrontal cortex in verbal processing: semantic processing or willed action? , 1994, Neuroreport.

[30]  Karl J. Friston,et al.  Anterior prefrontal cortex mediates rule learning in humans. , 2001, Cerebral cortex.

[31]  Uta Noppeney,et al.  Retrieval of abstract semantics , 2004, NeuroImage.

[32]  Lance J. Rips,et al.  Semantic distance and the verification of semantic relations , 1973 .

[33]  Jonathan D. Cohen,et al.  Prefrontal Cortex and the Flexibility of Cognitive Control : Rules Without Symbols , 2022 .

[34]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[35]  J. Fiez Phonology, Semantics, and the Role of the Left Inferior Prefrontal Cortex , 2022 .

[36]  W. F. Battig,et al.  Handbook of semantic word norms , 1978 .

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

[38]  K. C. Anderson,et al.  Single neurons in prefrontal cortex encode abstract rules , 2001, Nature.

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

[40]  David J. Freedman,et al.  Neural correlates of categories and concepts , 2003, Current Opinion in Neurobiology.

[41]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[43]  Alex Martin,et al.  Semantic memory and the brain: structure and processes , 2001, Current Opinion in Neurobiology.

[44]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.