Elsevier

Cortex

Volume 49, Issue 3, March 2013, Pages 611-625
Cortex

Review
The neural basis of semantic cognition: Converging evidence from neuropsychology, neuroimaging and TMS

https://doi.org/10.1016/j.cortex.2012.10.008Get rights and content

Abstract

Recent studies suggest that a complex, distributed neural network underpins semantic cognition. This article reviews our contribution to this emerging picture and traces the putative roles of each region within this network. Neuropsychological studies indicate that semantic cognition draws on at least two interacting components: semantic representations [degraded in semantic dementia (SD)] and control processes [deficient in patients with multimodal semantic impairment following stroke aphasia (SA)]. To explore the first component, we employed distortion-corrected functional magnetic resonance imaging (fMRI) and transcranial magnetic stimulation (TMS) in healthy volunteers: these studies convergently indicated that the anterior temporal lobes (ATLs; atrophied in SD) combine information from different modalities within an amodal semantic “hub”. Regions of cortex that code specific semantic features (“spokes”) also make a critical contribution to knowledge within particular categories. This network of brain regions interacts with semantic control processes reliant on left inferior frontal gyrus (LIFG), posterior middle temporal gyrus (pMTG) and inferior parietal cortices. SA patients with damage to these regions have difficulty focussing on aspects of knowledge that are relevant to the current goal or context, in both verbal and non-verbal tasks. SA patients with LIFG and temporoparietal lesions show similar deficits of semantic control, suggesting that a large-scale distributed cortical network underpins semantic control. Convergent evidence is again provided by fMRI and TMS. We separately manipulated the representational and control demands of a semantic task in fMRI, and found a dissociation within the temporal lobe: ATL was sensitive to the number of meanings retrieved, while pMTG and LIFG showed effects of semantic selection. Moreover, TMS to LIFG and pMTG produced equal disruption of tasks tapping semantic control. The next challenges are to delineate the specific roles of each region within the semantic control network and to specify the way in which control processes interact with semantic representations to focus processing on relevant features of concepts.

Section snippets

Neural basis of semantic representation

Where is semantic knowledge represented in the brain? Many researchers propose an ‘embodied’ view in which semantic information draws on a distributed network of sensory and motor representations (e.g., Pulvermuller, 2005; Martin, 2007; Barsalou, 1999). According to this view, the meaning of an item like “scissors” is derived from links between neural assemblies that represent this object's distinctive shape, the “snip” sound that it makes, information about how you hold and use scissors,

Deregulated semantic cognition in semantic aphasia

Studies of patients with SD have been enormously important in advancing our understanding the role of the ATL in semantic memory. However, deficits of semantic cognition are seen more frequently following left-hemisphere stroke. These patients typically implicate a different set of regions in semantic processing, most notably left posterior temporal, inferior parietal and inferior frontal regions (Chertkow et al., 1997; Berthier, 2001; Hart and Gordon, 1990; Hillis et al., 2001; Dronkers

Conclusion and future directions

Our research over the last 5 years has contributed to our understanding of the distributed neural network underpinning semantic cognition in several ways: (1) We have obtained convergent evidence from distortion-corrected fMRI and TMS studies of healthy volunteers that points to a role of both left and right ATL in the representation of word and picture meanings, in line with findings from investigations of patients with SD. (2) The distortion-corrected fMRI studies indicate graded

Acknowledgements

The work reported in this article would not have been possible without the efforts of my colleagues and collaborators: I have benefited enormously from their ingenuity and kindness. I am particularly indebted to Matt Lambon Ralph at the University of Manchester, who has provided me with invaluable support for many years. I would also like to extend special thanks to the following people who played a key role in particular projects: Azizah Almaghyuli, Richard Binney, Faye Corbett, Sheeba Ehsan,

References (145)

  • A.R. Damasio

    Category-related recognition defects as a clue to the neural substrates of knowledge

    Trends in Neurosciences

    (1990)
  • B. Desgranges et al.

    Anatomical and functional alterations in semantic dementia: A voxel-based MRI and PET study

    Neurobiology of Aging

    (2007)
  • J.T. Devlin et al.

    Susceptibility-induced loss of signal: Comparing PET and fMRI on a semantic task

    NeuroImage

    (2000)
  • J. Diehl et al.

    Cerebral metabolic patterns at early stages of frontotemporal dementia and semantic dementia. A PET study

    Neurobiology of Aging

    (2004)
  • N. Dronkers et al.

    Lesion analysis of the brain areas involved in language comprehension

    Cognition

    (2004)
  • J. Duncan

    The multiple-demand (MD) system of the primate brain: Mental programs for intelligent behaviour

    Trends in Cognitive Sciences

    (2010)
  • H. Goodglass et al.

    Frequency, picturability and availability of nouns in aphasia

    Cortex

    (1969)
  • M.L. Gorno-Tempini et al.

    Echo time dependence of BOLD contrast and susceptibility artifacts

    NeuroImage

    (2002)
  • O. Hauk et al.

    Somatotopic representation of action words in human motor and premotor cortex

    Neuron

    (2004)
  • P. Hoffman et al.

    Remembering ‘zeal’ but not ‘thing’: Reverse frequency effects as a consequence of deregulated semantic processing

    Neuropsychologia

    (2011)
  • C. Humphries et al.

    Time course of semantic processes during sentence comprehension: An fMRI study

    NeuroImage

    (2007)
  • M. Ikeda et al.

    A horse of a different colour: Do patients with semantic dementia recognise different versions of the same object as the same?

    Neuropsychologia

    (2006)
  • E. Jefferies et al.

    Refractory effects in stroke aphasia: A consequence of poor semantic control

    Neuropsychologia

    (2007)
  • E. Jefferies et al.

    A category-specific advantage for numbers in verbal short-term memory: Evidence from semantic dementia

    Neuropsychologia

    (2004)
  • E. Jefferies et al.

    Deficits of knowledge versus executive control in semantic cognition: Insights from cued naming

    Neuropsychologia

    (2008)
  • S. Luzzi et al.

    Distinct patterns of olfactory impairment in Alzheimer's disease, semantic dementia, frontotemporal dementia, and corticobasal degeneration

    Neuropsychologia

    (2007)
  • A. Mechelli et al.

    Semantic relevance explains category effects in medial fusiform gyri

    NeuroImage

    (2006)
  • L. Meteyard et al.

    Coming of age: A review of embodiment and the neuroscience of semantics

    Cortex

    (2012)
  • I.E. Nagel et al.

    Functional MRI investigation of verbal selection mechanisms in lateral prefrontal cortex

    NeuroImage

    (2008)
  • P.J. Nestor et al.

    Declarative memory impairments in Alzheimer's disease and semantic dementia

    NeuroImage

    (2006)
  • U. Noppeney et al.

    The neural areas that control the retrieval and selection of semantics

    Neuropsychologia

    (2004)
  • U. Noppeney et al.

    A PET study of stimulus- and task-induced semantic processing

    NeuroImage

    (2002)
  • J.M. Ogar et al.

    Semantic dementia and persisting Wernicke's aphasia: Linguistic and anatomical profiles

    Brain and Language

    (2011)
  • J. Ojemann et al.

    Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts

    NeuroImage

    (1997)
  • D. Perani et al.

    Word and picture matching: A PET study of semantic category effects

    Neuropsychologia

    (1999)
  • L.W. Barsalou

    Perceptual symbol systems

    Behavioral and Brain Sciences

    (1999)
  • M. Bedny et al.

    Concepts are more than percepts: The case of action verbs

    The Journal of Neuroscience

    (2008)
  • M. Bedny et al.

    Semantic adaptation and competition during word comprehension

    Cerebral Cortex

    (2008)
  • M.L. Berthier

    Unexpected brain–language relationships in aphasia: Evidence from transcortical sensory aphasia associated with frontal lobe lesions

    Aphasiology

    (2001)
  • J.R. Binder et al.

    Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies

    Cerebral Cortex

    (2009)
  • J.R. Binder et al.

    Conceptual processing during the conscious resting state: A functional MRI study

    Journal of Cognitive Neuroscience

    (1999)
  • J.R. Binder et al.

    Distinct brain systems for processing concrete and abstract concepts

    Journal of Cognitive Neuroscience

    (2005)
  • R.J. Binney et al.

    The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: Evidence from a novel direct comparison of distortion-corrected fMRI, rTMS and semantic dementia

    Cerebral Cortex

    (2010)
  • R.J. Binney et al.

    Convergent connectivity and graded specialization in the rostral human temporal lobe as revealed by diffusion-weighted imaging probabilistic tractography

    Journal of Cognitive Neuroscience

    (2012)
  • R.J. Binney

    Exploring the role of the anterior temporal lobe in semantic cognition. Doctoral thesis, School of Psychological Sciences

    (2010)
  • N.M. Borden

    3D Angiographic Atlas of Neurovascular Anatomy and Pathology

    (2006)
  • S. Bozeat et al.

    A duck with four legs: Investigating the structure of conceptual knowledge using picture drawing in semantic dementia

    Cognitive Neuropsychology

    (2003)
  • S. Bozeat et al.

    When objects lose their meaning: What happens to their use?

    Cognitive, Affective & Behavioural Neuroscience

    (2002)
  • M. Catani et al.

    The rises and falls of disconnection syndromes

    Brain

    (2005)
  • L.L. Chao et al.

    Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects

    Nature Neuroscience

    (1999)
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