Exploring the role of the posterior middle temporal gyrus in semantic cognition: Integration of anterior temporal lobe with executive processes

Making sense of the world around us depends upon selectively retrieving information relevant to our current goal or context. However, it is unclear whether selective semantic retrieval relies exclusively on general control mechanisms recruited in demanding non-semantic tasks, or instead on systems specialised for the control of meaning. One hypothesis is that the left posterior middle temporal gyrus (pMTG) is important in the controlled retrieval of semantic (not non-semantic) information; however this view remains controversial since a parallel literature links this site to event and relational semantics. In a functional neuroimaging study, we demonstrated that an area of pMTG implicated in semantic control by a recent meta-analysis was activated in a conjunction of (i) semantic association over size judgements and (ii) action over colour feature matching. Under these circumstances the same region showed functional coupling with the inferior frontal gyrus — another crucial site for semantic control. Structural and functional connectivity analyses demonstrated that this site is at the nexus of networks recruited in automatic semantic processing (the default mode network) and executively demanding tasks (the multiple-demand network). Moreover, in both task and task-free contexts, pMTG exhibited functional properties that were more similar to ventral parts of inferior frontal cortex, implicated in controlled semantic retrieval, than more dorsal inferior frontal sulcus, implicated in domain-general control. Finally, the pMTG region was functionally correlated at rest with other regions implicated in control-demanding semantic tasks, including inferior frontal gyrus and intraparietal sulcus. We suggest that pMTG may play a crucial role within a large-scale network that allows the integration of automatic retrieval in the default mode network with executively-demanding goal-oriented cognition, and that this could support our ability to understand actions and non-dominant semantic associations, allowing semantic retrieval to be ‘shaped’ to suit a task or context.

[1]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[2]  Hao-Ting Wang,et al.  Representing Representation: Integration between the Temporal Lobe and the Posterior Cingulate Influences the Content and Form of Spontaneous Thought , 2016, PloS one.

[3]  Robert T. Knight,et al.  Effects of frontal lobe damage on interference effects in working memory , 2002, Cognitive, affective & behavioral neuroscience.

[4]  Grant M. Walker,et al.  Neuroanatomical dissociation for taxonomic and thematic knowledge in the human brain , 2011, Proceedings of the National Academy of Sciences.

[5]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[6]  K. Patterson,et al.  Deficits of knowledge vs . executive control in semantic cognition : Insights from cued naming , 2008 .

[7]  Gina F. Humphreys,et al.  Fusion and Fission of Cognitive Functions in the Human Parietal Cortex , 2014, Cerebral cortex.

[8]  Jonathan D. Power,et al.  Control-related systems in the human brain , 2013, Current Opinion in Neurobiology.

[9]  Michael Wilson,et al.  MRC psycholinguistic database: Machine-usable dictionary, version 2.00 , 1988 .

[10]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[11]  M. L. Lambon Ralph,et al.  Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. , 2006, Brain : a journal of neurology.

[12]  A. Nobre,et al.  Dissociating Linguistic Processes in the Left Inferior Frontal Cortex with Transcranial Magnetic Stimulation , 2022 .

[13]  Miranka Wirth,et al.  Semantic memory involvement in the default mode network: A functional neuroimaging study using independent component analysis , 2011, NeuroImage.

[14]  M. L. Lambon Ralph,et al.  The Neural Organization of Semantic Control: TMS Evidence for a Distributed Network in Left Inferior Frontal and Posterior Middle Temporal Gyrus , 2010, Cerebral cortex.

[15]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[16]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

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

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

[19]  Paul Hoffman,et al.  The Semantic Network at Work and Rest: Differential Connectivity of Anterior Temporal Lobe Subregions , 2016, The Journal of Neuroscience.

[20]  Elizabeth Jefferies,et al.  Exploring multimodal semantic control impairments in semantic aphasia: Evidence from naturalistic object use , 2009, Neuropsychologia.

[21]  Nancy Kanwisher,et al.  Language-Selective and Domain-General Regions Lie Side by Side within Broca’s Area , 2012, Current Biology.

[22]  Theodoros Karapanagiotidis,et al.  Brain networks underlying bistable perception , 2015, NeuroImage.

[23]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[24]  Daniel S. Margulies,et al.  The default modes of reading: modulation of posterior cingulate and medial prefrontal cortex connectivity associated with comprehension and task focus while reading , 2013, Front. Hum. Neurosci..

[25]  Peter Hagoort,et al.  Effective connectivity of cortical and subcortical regions during unification of sentence structure , 2010, NeuroImage.

[26]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[27]  E. Jefferies,et al.  Anterior temporal lobes mediate semantic representation: Mimicking semantic dementia by using rTMS in normal participants , 2007, Proceedings of the National Academy of Sciences.

[28]  Leif D. Nelson,et al.  False-Positive Psychology , 2011, Psychological science.

[29]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[30]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[31]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[32]  J. Hodges,et al.  Non-verbal semantic impairment in semantic dementia , 2000, Neuropsychologia.

[33]  E. Jefferies The neural basis of semantic cognition: Converging evidence from neuropsychology, neuroimaging and TMS , 2013, Cortex.

[34]  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.

[35]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[36]  Elizabeth Jefferies,et al.  tegory-General Semantic Impairment Induced by Transcranial Magnetic Stimulation , 2010 .

[37]  Daniel S. Margulies,et al.  A Correspondence between Individual Differences in the Brain's Intrinsic Functional Architecture and the Content and Form of Self-Generated Thoughts , 2014, PloS one.

[38]  J. Binder,et al.  A comparison of five fMRI protocols for mapping speech comprehension systems , 2008, Epilepsia.

[39]  Richard S. J. Frackowiak,et al.  A voxel‐based morphometry study of semantic dementia: Relationship between temporal lobe atrophy and semantic memory , 2000, Annals of neurology.

[40]  Timothy E. J. Behrens,et al.  Tools of the trade: psychophysiological interactions and functional connectivity. , 2012, Social cognitive and affective neuroscience.

[41]  P. Hoffman,et al.  The Roles of Left Versus Right Anterior Temporal Lobes in Conceptual Knowledge: An ALE Meta-analysis of 97 Functional Neuroimaging Studies , 2015, Cerebral cortex.

[42]  Hongkeun Kim,et al.  Differential neural activity in the recognition of old versus new events: An Activation Likelihood Estimation Meta‐Analysis , 2013, Human brain mapping.

[43]  Brian R. Tietz,et al.  Deciding Which Way to Go: How Do Insects Alter Movements to Negotiate Barriers? , 2012, Front. Neurosci..

[44]  P. Matthews,et al.  Semantic Processing in the Left Inferior Prefrontal Cortex: A Combined Functional Magnetic Resonance Imaging and Transcranial Magnetic Stimulation Study , 2003, Journal of Cognitive Neuroscience.

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

[46]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[47]  Ellen F. Lau,et al.  Automatic Semantic Facilitation in Anterior Temporal Cortex Revealed through Multimodal Neuroimaging , 2013, The Journal of Neuroscience.

[48]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[49]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[50]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[51]  J. Smallwood,et al.  Automatic and Controlled Semantic Retrieval: TMS Reveals Distinct Contributions of Posterior Middle Temporal Gyrus and Angular Gyrus , 2015, The Journal of Neuroscience.

[52]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[53]  David Badre,et al.  Functional Magnetic Resonance Imaging Evidence for a Hierarchical Organization of the Prefrontal Cortex , 2007, Journal of Cognitive Neuroscience.

[54]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[55]  Tilo Kircher,et al.  Categorical and thematic knowledge representation in the brain: Neural correlates of taxonomic and thematic conceptual relations , 2008, Neuropsychologia.

[56]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[57]  M. A. Lambon Ralph,et al.  The inferior, anterior temporal lobes and semantic memory clarified: Novel evidence from distortion-corrected fMRI , 2010, Neuropsychologia.

[58]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[59]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[60]  Marc Brysbaert,et al.  Subtlex-UK: A New and Improved Word Frequency Database for British English , 2014, Quarterly journal of experimental psychology.

[61]  Elizabeth Jefferies,et al.  “Pre-semantic” cognition revisited: Critical differences between semantic aphasia and semantic dementia , 2010, Neuropsychologia.

[62]  J. Hodges,et al.  Semantic dementia: a unique clinicopathological syndrome , 2007, The Lancet Neurology.

[63]  Michael F. Bonner,et al.  Converging Evidence for the Neuroanatomic Basis of Combinatorial Semantics in the Angular Gyrus , 2015, The Journal of Neuroscience.

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

[65]  Haakon G. Engen,et al.  Shaped by the Past: The Default Mode Network Supports Cognition that Is Independent of Immediate Perceptual Input , 2015, PloS one.

[66]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

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

[68]  N. Kanwisher,et al.  A functional dissociation between language and multiple-demand systems revealed in patterns of BOLD signal fluctuations. , 2014, Journal of neurophysiology.

[69]  Scott T. Grafton,et al.  A distributed left hemisphere network active during planning of everyday tool use skills. , 2004, Cerebral cortex.

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

[71]  P. Hoffman,et al.  Ventrolateral Prefrontal Cortex Plays an Executive Regulation Role in Comprehension of Abstract Words: Convergent Neuropsychological and Repetitive TMS Evidence , 2010, The Journal of Neuroscience.

[72]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[73]  Elizabeth Jefferies,et al.  Conceptual control across modalities: graded specialisation for pictures and words in inferior frontal and posterior temporal cortex , 2015, Neuropsychologia.

[74]  Gina F. Humphreys,et al.  Establishing task- and modality-dependent dissociations between the semantic and default mode networks , 2015, Proceedings of the National Academy of Sciences.

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

[76]  Mia Liljeström,et al.  Perceiving and naming actions and objects , 2008, NeuroImage.

[77]  Margaret D. King,et al.  The NKI-Rockland Sample: A Model for Accelerating the Pace of Discovery Science in Psychiatry , 2012, Front. Neurosci..

[78]  Elizabeth Jefferies,et al.  Shared neural processes support semantic control and action understanding , 2015, Brain and Language.

[79]  Elizabeth Jefferies,et al.  Going beyond Inferior Prefrontal Involvement in Semantic Control: Evidence for the Additional Contribution of Dorsal Angular Gyrus and Posterior Middle Temporal Cortex , 2013, Journal of Cognitive Neuroscience.