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The neural and computational bases of semantic cognition

Key Points

  • Semantic cognition refers to our ability to use, manipulate and generalize knowledge that is acquired over the lifespan to support innumerable verbal and non-verbal behaviours.

  • Semantic cognition relies on two principal interacting neural systems: representation and control. We refer to this two-system view as the controlled semantic cognition framework.

  • Coherent, generalizable concepts are formed through the hub-and-spoke representational system with the hub localised to the anterior temporal region (bilaterally) and spokes localised in modality-specific association cortices that are distributed across the cortex.

  • Convergent clinical and cognitive neuroscience data show that the anterior temporal lobe hub has graded variations of semantic function that follow its pattern of connectivity.

  • Category-specific differences in semantic function reflect the contributions of different parts of the connectivity-constrained version of the hub-and-spoke framework.

  • Semantic control is implemented within a distributed frontal and temporoparietal neural network. Semantic control supports executive mechanisms that constrain how activation propagates through the network for semantic representation.

Abstract

Semantic cognition refers to our ability to use, manipulate and generalize knowledge that is acquired over the lifespan to support innumerable verbal and non-verbal behaviours. This Review summarizes key findings and issues arising from a decade of research into the neurocognitive and neurocomputational underpinnings of this ability, leading to a new framework that we term controlled semantic cognition (CSC). CSC offers solutions to long-standing queries in philosophy and cognitive science, and yields a convergent framework for understanding the neural and computational bases of healthy semantic cognition and its dysfunction in brain disorders.

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Figure 1: The original hub-and-spoke model.
Figure 2: The graded ATL semantic hub.
Figure 3: The neural basis of semantic control.

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Acknowledgements

The authors are indebted to all of the patients and their carers for their continued support of the research programme. This research was supported by an MRC Programme grant to M.A.L.R. (MR/J004146/1). E.J. was supported by a grant from the European Research Council (283530-SEMBIND).

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Supplementary information

Supplementary information S1 (figure)

Convergent evidence for the critical role of the ATL in semantic function (PDF 1766 kb)

Supplementary information S2 (figure)

Differential effect of typicality in SA vs. SD patients (PDF 1766 kb)

Supplementary information S3 (figure)

Convergent evidence for the multimodal nature of the ATL semantic function (PDF 1766 kb)

Supplementary information S4 (figure)

Convergent evidence for the timing of semantic function in the ATL region (PDF 1766 kb)

Supplementary information S5 (figure)

Evidence for the division of representational labour across the hub and spokes. (PDF 1766 kb)

Supplementary information S6 (figure)

Parallel verbal and nonverbal semantic control deficits in semantic aphasia (PDF 1766 kb)

Supplementary information S7 (figure)

Qualitatively-different semantic impairment in SA vs. SD patients (PDF 1766 kb)

Supplementary information S8 (figure)

The modulatory influence of positive vs. negative cues on word ambiguity effects in SA patients. (PDF 1766 kb)

PowerPoint slides

Glossary

Concepts

Conceptual knowledge or semantic memory (typically treated as being synonymous terms in cognitive neuroscience) refers to our lifelong acquired, multimodal knowledge of, for example, objects, people, facts and words.

Semantic dementia

(SD). This is the temporal lobe variant of frontotemporal dementia and is characterised by progressive but relatively selective degradation of semantic knowledge and by hypometabolism and atrophy that are centred on the anterior temporal lobe (this is always bilateral, although often asymmetrical early in the disease).

Electrocorticography

Implanted grid or depth electrodes that are used to record local field potentials.

18F-fluorodeoxyglucose positron emission tomography

An imaging technique that is used to measure the rate of glucose metabolism across the brain.

Transcranial magnetic stimulation

(TMS). Electromagnetic coils are placed over the scalp to stimulate the underlying cortex. The frequency, intensity and duration of pulses can be varied to induce inhibition or excitation.

U-fibre connections

Short-range white-matter fibres that connect two local, neighbouring areas. The profile of such fibres is often a 'U' shape — hence the name. Such fibres contrast with white-matter fasciculi, which comprise large bundles of white-matter fibres that connect distant regions.

Herpes simplex virus encephalitis

(HSVE). An acute or subacute infection in the brain that is often transmitted via the olfactory nerve and typically causes damage to the anterior temporal lobes.

Semantic aphasia

(SA). A condition affecting patients who, after acute brain damage (usually from stroke), show deficits in verbal but also non-verbal semantic tasks, as well as in other cognitive domains that require executively linked manipulation of internally represented knowledge.

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Ralph, M., Jefferies, E., Patterson, K. et al. The neural and computational bases of semantic cognition. Nat Rev Neurosci 18, 42–55 (2017). https://doi.org/10.1038/nrn.2016.150

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